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Mechanisms and physiological role of polarity in plants

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DOI: 10.1134/s1021443712040085

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ISSN 10214437, Russian Journal of Plant Physiology, 2012, Vol. 59, No. 4, pp. 502–514. © Pleiades Publishing, Ltd., 2012.
Original Russian Text © S.S. Medvedev, 2012, published in Fiziologiya Rastenii, 2012, Vol. 59, No. 4, pp. 543–556.

REVIEWS

Mechanisms and Physiological Role of Polarity in Plants

S. S. Medvedev
Department of Plant Physiology and Biochemistry, St. Petersburg State University,
Universitetskaya nab. 7/9, St. Petersburg, 199034 Russia;
fax: 7 (812) 3289703; email: ssmedvedev@mail.ru
Received June 25, 2011

Abstract—The concept of polarity was the starting point for the attempts of many investigators to understand
the principles of differentiation, because the polar organization underlies specific threedimensional struc
ture of the organism and provides for the integrity and coordination of its functions. The polarity axes are
established at the stage of zygote, extending to the developing embryo, and they “vectorize” subsequent plant
growth and development. Polarization of cells and tissues is crucial for plant morphogenesis, because the
emerging morphogenetic gradients provide the basis for differential genome activity at various stages of plant
development. This review deals with the polarity phenomena and the mechanisms of symmetry axis forma
tion at the level of cells and plant tissues. The roles of electrical gradients, Ca2+ ions, auxin, cytoskeleton,
ROPproteins, phosphoinositides, and microRNA in polarization of cells and tissues are considered.

Keywords: higher plants, growth and morphogenesis, polarity, physiological gradients, polar IAA transport,
bioelectric potential gradients, polar Ca2+ fluxes, cytoskeleton, ROPGTPases, microRNA.
DOI: 10.1134/S1021443712040085

INTRODUCTION particular [1, 2]. A distinctive feature of polarizing

Activities of individual organs, tissues, and cells in
any multicellular organism should be coordinated in
order to enable integrated functioning of the organism
as a whole. One of the most essential elements of plant
integrity is polarity, i.e., the axial spatial organization
of plant body. The term polarity means specific orien
tation of plant activity and morphogenesis in space.
Polarity can be also defined as the existence of function
ally significant asymmetric structures that are formed in
response to vectorial cues (external or internal).
The axial polarity implies the presence of a well
developed longitudinal axis bearing lateral organs, i.e.,
lateral branches and roots, leaves, and flowers. The
axially organized growth of cells and tissues precludes
the formation of a shapeless bulk of living matter. All
plant organs and tissues are initiated symmetrically
along the plant axes. In addition to axial polarity, dor
soventral and radial polarities are also distinguished.
Nevertheless, the term polarity denotes in most cases
the axial polarity.
Polarization can be induced by physical factors
(light, gravity, electric and magnetic fields) and by
chemical agents (hormones, ions). Particularly effec
tive means of cell polarization is the creation of local
ion gradients, the gradients of Ca2+, K+, and H+ in
Abbreviations: BEP—bioelectric potentials; IP3—inositol 1,4,5
trisphosphate; NPA—naphthylphtalamic acid; TIBA—2,3,5tri
iodobenzoic acid.
cues is their directional (vectorial) mode.
CELL BASES OF POLARITY
Possible mechanisms of polarization at the plant
cell level were first considered by Bentrup [2] and
Schnepf [3]. They believed that polarization is basi
cally related to axial gradients of bioelectric potentials
(BEP) arising from changes in membrane ionic per
meability, primarily to Ca2+, K+, Cl–, and H+. The
polar cell growth, e.g., growth of pollen tubes or root
hairs, is characterized by several features such as the
cytosolic Ca2+ gradient focused in the direction of
growth, polarization of the actin cytoskeleton, and the
apical transport of membrane vesicles with their sub
sequent exocytosis. The formation of symmetry axes
in plant cells involves also monomeric GTPbinding
proteins, phosphoinositides, and Cadependent pro
tein kinases [4].
Electric Polarization of the Plant Cell
The electrophysiological polarity axis of the
nascent plant is established at the earliest stages of
plant development. Within 30 min after fertilization,
the zygote of a brown alga Fucus becomes electrically
polarized. At this stage, the inward electric current was
recorded in the nascent rhizoid area and the outward
current was observed on the opposite cell side where
the incipient thallus emerged. The highest density of

502
 MECHANISMS AND PHYSIOLOGICAL ROLE OF POLARITY IN PLANTS
(а) (b)
100 µm
Fig. 1. Distribution of electric current lines.
(a) Germinating Fucus zygote; (b) germinating pollen grain of lily; (c) the root and root hair of barley [2]. Arrows indicate the
direction of movement of positive charges.
the electric current was detected in the region of
intensely growing rhizoid pole (Fig. 1). The axial gra
dients of bioelectric potentials were also found in
growing pollen tubes, elongating root hairs, and devel
oping embryoids and root tips [2, 5].
The appearance of inward electrical currents in the
growing cell regions and of outward currents in the cell
areas that have stopped growing is the earliest event in
the process of cell differentiation. These electrical cur
rents usually precede morphological changes and are
carried by ion species, such as Ca2+, K+, Cl–, and H+
[5, 6]. Using Ca2+selective vibrating microelectrodes,
Pierson et al. [7] detected the Ca2+ currents along the
growing lily pollen tube. The elongating pollen tube
was characterized by a specific profile of Ca2+current,
the highest density of inward current was observed in
the region of intensely growing apex.
The study of differentiation of Fucus zygotes
revealed that unidirectional environmental factors,
such as gravity and light, produce the local increase in
calcium permeability of the plasma membrane, lead
ing to membrane depolarization on the nascent rhiz
oid pole of the zygote [5, 8]. Local changes in mem
brane potential give rise to electric polarization of the
cell, cytoplasmic ion gradients, rearrangements of the
cytoskeleton, and fixation of cell polarity axis. When
the zygote divides perpendicularly to the main axis,
the nuclei of daughter cells become surrounded by the
cytoplasm existing in different functional states;
therefore, these nuclei start implementing different
genetic programs [9].
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
503
(c)
100 µm
Ca2+ Gradients in the Plant Cell
The emission of fluorescent probes loaded into the
cells exhibiting polar growth (pollen tubes, root hairs,
fungal hyphae) revealed the existence of tipfocused
Ca2+ gradient with Ca2+ concentration decreasing
from the apex to the cell base. The cytosolic calcium
level is particularly high in intensely growing cell api
ces. The axial gradient of ionized calcium in lily pollen
grains and pollen tubes was first discovered following
the microinjection of the fluorescent Ca2+ probe fura
2–dextran [7]. In pollen grains the highest calcium
gradient was observed just before the formation of the
pollen tube. The pollen tube is characterized by its
own Ca2+ gradient, with Ca2+ concentration increas
ing from the tube base to the tip. The Ca2+ concentra
tion in the apical zone of pollen tube was about 3 µM,
whereas at a distance of 20 µm from the tip it reduced
to 0.2 µM. The entry of calcium ions into the pollen
tube is thought to occur through the Ca2+ channels
localized in the apical cell part. It was found that the
cytoplasmic calcium gradient oscillates and moves
along the pollen tube in the direction of growing apex.
The cytoplasmic Ca2+ concentration was found to
oscillate synchronously with growth rate oscillations
in the pollen tube [10]. The experimental dissipation
of the cytoplasmic Ca2+ gradient was accompanied by
the cessation of pollen tube growth.
Fucoid eggs have no discernible cellular asymme
tries at the initial stage. Their organelles are randomly
oriented, and short rods of Factin are evenly distrib
Vol. 59 No. 4 2012
504 MEDVEDEV
uted throughout the cortex over the cell perimeter
[11]. Subsequent structural changes, occurring after
fertilization of the egg cell, are caused primarily by
local increase in the cytoplasmic Ca2+ level, which
immediately arises beneath the plasma membrane at
the sperm entry site.
The gradient of Ca2+ concentration, decreasing
from the cell apex to the cell base, seems to be indis
pensible for the normal function of cells exhibiting
apical growth. Dissipation of intracellular Ca2+ gradi
ents by treating the cells with chelators, exogenous
calcium, or the calcium ionophore A23187 led to ces
sation of apical growth and caused in some cases the
dispersed distribution of organelles in the initially
polar cell structures [7, 12].
Summing up the above discussion, it should be
noted that Ca2+ gradients carry the primary informa
tion about emerging polarization vectors. The build
up of the intracellular Ca2+ gradient is followed by the
emerging gradients for Ca2+binding sensor proteins
and Ca2+dependent protein kinases, which leads to
spatially inhomogeneous activity of many enzymes
[13]. Thus, secondary (e.g., secretory and metabolic)
gradients may arise. Finally, the Ca2+sensitive cytosk
eletal elements accomplish the structural cell polariza
tion (Fig. 2).
Cytoskeleton
The cytoskeleton of plant cells includes the tubu
lincomposed microtubules, the actin filaments
(microfilaments), and the myosinlike proteins and
actinbinding proteins. Plant cells contain also a series
of intermediate filament proteins. However, the forma
tion of typical intermediate filaments, characteristic of
animal cells, has not been revealed in plants. The
cytoskeleton is a crucial polarizing structure, imple
menting the spatial orientation and coordination of
many processes; it largely determines the cell shape
[14]. Impairing the dynamics of actin microfilaments
by cytochalasin D or latrunkulin B was shown to dis
turb the cell shape in epidermis and hypocotyls, as well
as in root hairs and trichomes.
Individual cytoskeletal elements are not only inter
connected via specific proteins but can be also linked
to membrane structures. The membrane–skeleton
complex is a dynamic system that is sensitive to the
Ca2+ level, pH, ATP content, and a number of other
chemical and physical factors. The plant cell cytoskel
etal structures integrated into the membrane–skeleton
complex can act as immediate sensors of polarizing
signals. The relative stability and lability of the mem
brane–skeleton complex provides a duality to its func
tions: this complex provides for both maintenance and
modulation of forms and mutual positions of the cell
components [15]. This property of the cytoarchitec
tonics allows the cell to effectively control the cell
polarization processes. The asymmetry of plasmale
mma–cytoskeleton complex in polarized cells is man
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
ifested in asymmetric distribution of membrane chan
nels and ion pumps, as well as in vectorial ion transport
[7, 16], generation of electrical gradients [5], and,
eventually, in the polar growth.
Microtubules and actin filaments in the Fucus
zygote are initially distributed randomly. As the zygote
polarization progresses toward the first division, the
actin filaments accumulate in the apical cortex, where
they play an important role in elongation of the incip
ient “rhizoidal” cell. Microtubules are arranged radi
ally at this stage, thus determining the plane of cell
division [11, 14].
In addition to Ca2+ ions and electrical gradients,
cytoskeleton plays an important role in pollen grain
germination and polar growth of the pollen tube. The
orientation of cytoskeleton entails the polar distribu
tion of ion channels, which largely predetermines the
direction of pollen tube growth [14, 17].
The structure and function of actin filaments is
impaired by various cytochalasins. Analysis of cytoch
alasin action on differentiation of Fucus and Pelvetia
zygotes showed that the fibrillar actin plays a key role
in cell polarization and maintaining the axial anisot
ropy of cell morphogenesis [18]. The addition of
cytochalasin B, which inhibits polymerization and
function of actin filaments, disarranged the normal
orientation of cortical cytoskeleton and caused the
appearance of unnatural profiles in the developing alga
Pelvetia wrightii. The earliest disorders consisted in the
disruption of egg and embryo polarization [18]. The
treatment with cytochalasins completely inhibited the
electrophysiological polarization of the zygote, but
this inhibition was reversed after cell washing [19].
In our studies, we analyzed reorganization of the
actin cytoskeleton in gravistimulated Arabidopsis
roots (rotation of the plant position by 90°) [20]. In the
stele of the root elongation zone, the actin cytoskele
ton was represented by thick relatively straight bundles
that were oriented axially prior to gravistimulation.
The structure of the actin cytoskeleton changed signif
icantly within 15 min after the onset of gravistimula
tion: the microfilaments became fragmented and
curved, and their axial orientation was disturbed. After
30 min of gravistimulation, the actin microfilaments
remained curved but regained their predominant axial
orientation. After 60 min of gravistimulation, the actin
cytoskeleton of stele cells was similar to the cytoskele
ton of the control plants; however, individual microfil
aments were still bent. These rearrangements of the
actin microfilament network in the elongation zone of
gravistimulated roots indicate the possible involve
ment of actin in early events of the plant gravitropic
response, which precede the appearance of the auxin
lateral gradient and occur in advance of the growth
response.
The involvement of microtubules in establishing
cell polarity was demonstrated in many studies
employing colchicine. This alkaloid at micromolar
concentrations binds to tubulin and blocks its poly
Vol. 59 No. 4 2012
 MECHANISMS AND PHYSIOLOGICAL ROLE OF POLARITY IN PLANTS 505

Polarizing factors

microRNA ROPproteins PLC, PLD Ca2+channels

micro Actin IP3 PA Gradients of

tubules microfi Ca2+
цит

Polarization of PINprotein Potassium and Ca2+АТФазы Ca2+sensors

cellulose recyclin anion
microfibrills channels Ca2+/H+exchangers

mRNA cleavage, Polar secretion of Polar ion transport, Polar Ca2+dependent

blockage of proteins into BEP gradients Ca 2+ protein kinases
translation the plasmalemma fluxes in tissues

Polar fluxes and gradients of IAA in tissues

Po l a r g r o w t h , d i f f e r e n t i a t i o n , m o r p h o g e n e s i s

Fig. 2. Processes underlying polarity of plant cells and tissues.

2+
PLC—phospholipase C; PLD—phospholipase D; IP3—inositol 1,4,5trisphosphate; PA—phosphatidic acid; Ca cyt —cyto
plasmic concentration of ionized calcium; BEP—biolelectric potentials.

merization. Higher concentrations of colchicine (> 1
mM) depolymerized the microtubules. The treatment
with colchicine was shown to disrupt the polar pattern
formation of root hair cells in the trichoblasts of Gibe
sis gemiculata and Tradescantia fluminensis [21].
The organization of cortical microtubules is
strongly affected by Ca2+ and H+, hormones, and bio
electric potential gradients [22, 23]. Application of
weak electrical fields and mechanical pressure can
reorient the cortical microtubules, whose direction
became perpendicular to the applied field already after
6h treatment [22]. The Ca2+ and H+ ions are involved
in regulation of assembling (and disassembling) of not
only microtubules but also actin filaments [24, 25].
The calciumdependent functioning of the cytosk
eleton in plant organisms is involved in many pro
cesses, such as movement of chloroplasts and flagella,
cyclosis, cell division, and polar cell growth. Some
researchers suppose that Ca2+ ions are needed for
polar growth (e.g., pollen tube growth), because they
control the operation of cytoskeleton [17]. However, the
structure of the cytoskeleton is regulated not only by cal
cium ions, but also by second messengers, such as inosi
tol 1,4,5trisphosphate (IP3) and cytosolic pH [17].
It was found that, at early developmental stages of
the Pelvetia zygote, the pH in the area of emerging
rhizoid is shifted by 0.1 units to the acidic direction, as
compared to pH in other cell parts [26]. This cytoplas
mic pH gradient is almost superimposed over the Ca2+
gradient and clearly correlates with the growth rate of
the emerging rhizoid. The pH gradients are assumed
to promote cell polarization by exerting local control
over assembling (and disassembling) of cytoskeletal
elements. It is established that the fibrillar actin is sta
bilized at a high concentration of H+ ions [25],
whereas microtubules are comparatively stable at a low
concentrations of H+ and Ca2+ [24].
Orientation and activity of the cytoskeleton in
plants depends on the plant hormonal status [23]. It is
assumed that the polar flow of auxin is able to initiate
the transverse orientation of microtubules with respect
to the main cell axis. This would cause the transverse
arrangement of cellulose microfibrils and, conse
quently, the axial orientation of the cells. Bergfeld et
al. [27] applied scanning electron microscopy to
investigate the reorientation of microtubules and cel
lulose microfibrils in epidermal cell walls of maize
coleoptiles during auxininduced growth. They
showed that the depletion of endogenous auxin ele
vated the proportion of microtubules and cellulose
microfibrils oriented parallel to the main cell axis.
Stimulation of growth by means of exogenous auxin
was followed within 30–60 min by the increase in the
number of microtubules and microfibrils oriented in
the transverse direction.
Auxin was found to induce the transverse orienta
tion of microtubules in Phaseolus azuki epicotyls even
under anaerobic conditions when the epicotyl growth
was almost stopped [28]. These results provide indirect
evidence that the effect of auxin on the orientation of

RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 59 No. 4 2012

506 MEDVEDEV
tubulin cytoskeleton is apparently unrelated to the
influence of IAA on growth. This notion clarifies why
the colchicine treatment had little influence on
growthactivating impact of auxin [23]; i.e., the auxin
mediated regulation of plant cell growth is apparently
unrelated to its effect on the orientation of microtu
bules. Two proposals were suggested to explain the
above results: (1) the earliest stages of auxinactivated
growth are unrelated to microtubule reorientation and
(2) the action of auxin on cell elongation comprises
both colchicinesensitive and colchicineindependent
processes [29]. The early stages of IAA action are due
to “modification” of cell wall components, while the
later stages are caused by IAAmediated reorientation
of microtubules.
The orientation of microtubules is also influenced
by other phytohormones. For example, the treatment
with gibberellin induced the transverse alignment of
microtubules (relative to the longitudinal axis), thus
affecting the orientation of cellulose fibrils in cell walls
[30]. The treatment with kinetin and ABA rearranged
the transversely aligned microtubules and cellulose
microfibrils to the longitudinal alignment. Water
stress, known to elevate the ABA level and inhibit
growth, shifted the orientation of microtubules from
transverse to longitudinal alignment [23]. The gaseous
hormone ethylene also rearranged microtubules from
the transverse to longitudinal orientation as early as 30
min after the treatment [31].
ROPGTPases
It is known that actindependent processes, such as
establishment of cell polarity and cell differentiation,
can be controlled by GTPases of Rho family [32]. In
plants a new type of Rho GTPases was identified and
named ROPGTPases (abbreviation from Rho of
Plants). The ROPtype GTPases are a group of mono
meric GTPbinding proteins (mGproteins) that bind
and hydrolyze GTP [33].
The largest progress in understanding the role of
ROPproteins was achieved by studying the mecha
nisms involved in growth of pollen tubes and root hairs
[34]. Immunofluorescence and confocal microscopy
studies revealed that ROP1GTPase is expressed in
pollen grains and pollen tubes. The ROR protein was
concentrated in the cortical region of the pollen tube
apex and over the periphery of generative cell [35]. The
cortical ROP protein in the apex forms a gradient with
the concentration decreasing from the tip to the base.
This protein, apparently associated with the plasma
membrane, participates in the formation of the axial
Ca2+ gradient and controls the configuration of actin
cytoskeleton. The results indicate that the apical
ROPGTPase is involved in the signaling mechanism
that controls the actindependent polar growth of pol
len tubes mediated by Ca2+ and phosphoinositides
[36]. In epidermal leaf cells of Arabidopsis, the pro
teins ROP2 and ROP4 facilitate the assembling of
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
actin but disrupt the microtubular arrays by inactivat
ing the protein RIC1 associated with microtubules.
The protein ROP6 acts in the opposite manner: its
binding to RIC1 stabilizes the structure of cortical
microtubules.
Another important function of ROP proteins is
regulation of polar localization of auxincarrier pro
teins in the plasma membrane and the control of IAA
polar transport in plant tissues [37].
Phosphoinositides
The membrane lipids phosphoinositides and their
derivatives are important elements in regulation of
polar growth of plant cells [38]. The apical areas of
plasma membrane in growing pollen tubes and root
hairs are enriched with phosphoinositides (phosphati
dylinositol4,5bisphosphate) and with enzymes that
hydrolyze these phospholipids (phospholipases D and
C), thereby releasing the second messengers IP3 and
phosphatidic acid. The release of IP3 and phosphatidic
acid would activate the calcium permeability, thus cre
ating the cytoplasmic gradients of ionized calcium
2+
( Ca cyt ). Mutations damaging to proteins responsible
for phosphoinositide transport were found to disturb
the polar organization of fibrillar actin network, the
polarity of vesicular secretion, the axial gradient of
cytosolic calcium and, consequently, the polar cell
growth [39]. This means that phosphoinositides are
necessary for almost all processes underlying the regu
lation of polar growth in plant cells.
Thus, the gradients of BEP and Ca2+ ions provide
the primary physiological basis of polarity in plant
cells. The cytoskeleton, the monomeric GTPbinding
proteins, and phosphoinositides also contribute signif
icantly to the formation of the symmetry axes in plant
cells (Fig. 2). The cell polarization can also be caused
by mechanical tension, e.g., by local contacts with
other cells, extracellular materials, or substrates.
POLARITY OF PLANT ORGANS AND TISSUES
Plant organisms are characterized by the presence
of a longitudinal axis with different organs emerging
along its length: the root system is formed at one end
of the main axis and the shoot is formed at the other.
Thus, the axial morphological structure and the polar
organization of plants and plant organs are selfevi
dent. However, the processes underlying interactions
of cells, tissues, and organs during formation of the
axial symmetry in higher plants are scarcely known to
date.
Gradients of Bioelectric Potentials
Comparatively simple and uniform distributions of
growth rates and metabolic activities within individual
organs and tissues of a plant organism account for the
Vol. 59 No. 4 2012
 MECHANISMS AND PHYSIOLOGICAL ROLE OF POLARITY IN PLANTS
existence of clearly evident metabolic gradients,
which in turn give rise to the gradients of BEP. Electri
cal gradients of metabolic origin are recorded along
the roots, leaves, shoots, and the whole organism.
These gradients, reflecting different resting potentials
of various cells, are related to different rates of ion
transport, growth, photosynthesis, and respiratory
exchange [40]. Stress treatments (e.g., drought, low
temperature, clinorotation, and hypogravity) reduce
the axial gradients of bioelectric potentials. However,
when the original electrical polarity was restored by
passing a weak electric current, the growth rates in
control and treated plants became quite similar.
The organ apices and tissues with high physiologi
cal activity (cambium, root elongation zone) are usu
ally electronegative [5, 40, 41]. For example, in verti
cally oriented barley roots, the electrical current had
an outward direction in the root hair zone and was
directed inward in the elongation zone (Fig. 1); i.e.,
the current entered the negatively charged root part
exhibiting the highest growth rate [42].
Brawley et al. [43] measured BEP in differentiating
embryoids of wild carrot. Already at the globule stage,
the electric field was detected around the embryo. The
pattern of electric field lines was quite specific and
persisted throughout the embryo development. The
largest density of inward current was recorded in the
area of emerging cotyledons, whereas the peak of out
ward current was confined to the region of nascent
root apical meristem. The density of electric current in
the aforementioned areas was found to increase at
each new stage of the embryo development.
When the shoots of various plant species were
reoriented from the vertical to horizontal position
(gravistimulation), the transverse electric polarization
was found to arise. The upper part of an organ became
more negative than the lower organ part [44].
When the electric field was scanned with a vibrating
electrode, the electrical currents were detected in the
developing primary roots of wheat, oat, bean, peanut,
and lily plants, and in adventitious roots of potato
[45–47]. The inward electric current was observed in
the meristematic and elongation zones, whereas the
outward current was recorded in the areas that have
completed their growth. In studies with root tips of pea
plants, the inward electrical currents with the density
of about 1 µA/cm2 were observed in the meristematic
and elongation zones, and the outward currents of the
order of 0.1 µA/cm2 were recorded in the root hair
zone (cf. Fig. 1).
Thus, differentiation of zygote and embryo, as well
as rhizogenesis and gravitropic responses are associ
ated with electrical currents and with emergence of a
specific pattern of electric field lines. This electrical
pattern represents an integral characteristic of the
polarization upon growth and during formation of
plant organs and tissues.
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 59
507
In our studies with maize coleoptiles and pea inter
nodes [48] we analyzed the involvement of BEP gradi
ents in regulation of growth. By passing the electric
current with a strength of 1–6 µA through the seg
ments of maize coleoptiles and pea internodes in the
longitudinal direction, we found the increase in elon
gation rate when the segment apical part was con
nected to the anode pole. When the apical part was
connected to the cathode (the reverse direction of
electric current), we observed no significant change in
the growth rate. The activating effect was observed
after a lag period of 2.5 min on the average and
increased in proportion to the strength of electric cur
rent. When the electric current was turned off, the
growth rate returned to its original value. The inhibi
tors of polar auxin transport, i.e., naphthylphtalamic
acid (NPA) and 2,3,5triiodobenzoic acid (TIBA)
suppressed the stimulating effect of electric current on
growth. Hence, the accelerated elongation of plant
axial organ segments under the influence of an electric
current might be associated with changes in active
basipetal transport of IAA.
While studying the influence of electric current (6
µA) on transport of labeled auxin (14CIAA) and
endogenous IAA in the segments of maize coleoptiles,
we found that the rate of basipetal auxin transport
increased when the apical segment part was connected
to the anode [48]. Conversely, when the apical part of
coleoptiles was charged negatively by the connection
to the cathode, the movement of IAA in the basipetal
direction decelerated. In coleoptile segments treated
with NPA and TIBA (inhibitors of polar auxin trans
port), the stimulating effect of electric current on the
transport of 14CIAA was not observed. Thus, the
external electric field affected the basipetal transport
of exogenous 14CIAA and endogenous auxin. In both
cases, the passage of electric current through the plant
tissue stimulated the transport of IAA in the direction
of the negative electrode.
Polar Transport of IAA
Among all phytohormones, only IAA is distin
guished by the pronounced polar movement in plant
organism tissues. By creating the positional informa
tion, IAA concentration gradients act as a potent mor
phogenetic factor and play the central role in forma
tion of symmetry axes in higher plants at the organism
level. The vectorial (polar) transport of auxin underlies
the regulation of almost all morphogenetic processes
[49]. The polar auxin fluxes control embryogenesis
and apical dominance, the formation of buds and
shoots, phyllotaxis and defoliation, flowering and tro
pisms, and the formation vascular system and lateral
roots.
The main polar flow of auxin in the shoots and
roots is directed downwards; the auxin is primarily
transported through the cells of cambium, phloem,
and the xylem parenchyma. The polar auxin transport
No. 4 2012
508 MEDVEDEV
is an active process driven at the expense of energy. It
is decelerated under hypoxia and after the treatment
with inhibitors of respiration and protein synthesis.
Specific inhibitors of polar auxin transport are often
termed phytotropins, because they suppress the photo
induced and gravitropic responses. The phytotropins
of the natural origin include some flavonoids, namely,
quercetin, apigenin, and kaempferol. In the laboratory
practice, synthetic compounds such as NPA and TIBA
are often used [50].
The mechanism of auxin membrane transport is
often explained in terms of the chemiosmotic hypothesis
[51]. The essential point is that the weak acid IAA (pK
4.75) is 50% dissociated in the slightly acidic environ
ment of the cell walls and intercellular spaces (at pH
4.75). Undissociated auxin molecules are lipophilic
and readily permeate through the membrane along the
concentration gradient. Once the auxin entered the
cytoplasm, where pH is slightly alkaline, the major
part of IAA molecules dissociate into H+ and the
anion IAA–. The protons are excreted from the cell by
means of the H+ATPase. The auxin accumulation in
the cytoplasm builds up the concentration gradient
that forces IAA– anions to leave the cell. However,
IAA– anions are insoluble in membrane lipids and
cannot freely diffuse through the plasmalemma. The
auxin becomes “trapped,” since its efflux from the
cells can be only mediated by special membrane trans
porters.
The entry of IAA into the cell is facilitated by
AUX1/LAX proteins (auxin resistant 1/like AUX1
proteins), which are homologues of the amino acid
transporters [52, 53]. The cell uptake of IAA occurs in
the symport with proton uptake. The auxin extrusion
from the cells involves two types of carriers: PINpro
teins and some phosphoglycoproteins, such as PGP1
and PGP19 (abbreviations from Pglycoproteins)
[54]. These phosphoglycoproteins perform the ATP
dependent auxin transport. The PGP1 and PGP19
proteins integrated into the membrane possess two
ATPbinding domains; for this reason they are
assigned to the ABCfamily of membrane transporters
(abbreviation from ATPbinding cassettes).
The main transporters involved in the polar auxin
flow and the IAA efflux from the cells belong to a fam
ily of proteins called PIN (pinformed) in the case of
Arabidopsis, because the mutants deficient in these
proteins produce hairpin stems devoid of leaves and
flowers [55]. Furthermore, pin mutants are insensitive
to phytotropins and poorly sensitive to gravistimula
tion. The Arabidopsis plants were found to contain
eight genes encoding this type of auxin transporters
[56]. Owing to different membrane location of pro
teins from this family, the polar auxin transport in
plants may proceed in various directions. For example,
in the 2cell stage embryo, the PIN7 protein localized
on the apical part of plasma membrane of the suspen
sor cells enables the delivery of IAA into the embryo.
At the same time, the PIN1 protein residing at the
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
plasma membrane lateral surface equalizes IAA con
centrations in two embryo cells. At the globule stage,
the PIN1 protein together with PIN4 supplies the syn
thesized IAA from the embryo apex into the hypophy
sis (the uppermost cell of the suspensor). Different
localization of PIN1 in the cells of the tunic and the
body determines the directions of auxin flow in the
apical meristem of the shoot to the places of initiation
of leaf primordia. In root tips, the proteins PIN1,
PIN4, and PIN7 support the downward flow of auxin
along the stele, whereas the carrier PIN3 redistributes
the auxin flows in the lateral direction. At the same
time, PIN2 localized in the upper part of the plasma
membrane of cortex and epidermis cells, directs the
auxin flow from the root apex to its base [56–58].
Therefore, in the root apical meristem, the direction
of polar auxin transport has a shape of an inverted
umbrella.
The polar transport of IAA in plant tissues results
from the polar intracellular distribution of PINpro
teins carried by vesicular transport along the actin
microfilaments. Therefore, the polar auxin transport is
blocked by the fungal toxin brefeldin A inhibiting the
vesicular secretion, as well as by cytochalasin D and
latrunkulin B causing depolymerization or fragmenta
tion of Factin [59–61].
It is established that the distribution of PINpro
teins within the cell is provided by four processes [55]:
(1) primary exocytosis and uniform distribution in the
plasmalemma, (2) endocytosis (internalization) of
vesicles containing PINproteins, and their inclusion
into the endomembranes, (3) secondary exocytosis of
vesicles carrying PINproteins and their inclusion in
specific areas of the plasma membrane, and (4) vesic
ular transport of PINproteins to proteasomes for sub
sequent proteolysis.
De novo synthesized proteins PIN1 and PIN2 are
first delivered by exocytosis to the plasma membrane
and are uniformly distributed over this membrane
[62]. Then, the vesicles containing PIN proteins are
separated from the plasma membrane and included
into the endomembranes. Thereafter, they are directed
by reexocytosis to the certain parts of the plasma
membrane (PIN1 is transported to the basal and PIN2
to the apical cell parts). The vector for exocytosis of
PIN proteins is determined by ARF/GEF factors
(abbreviation from adenosyl ribosylation factor and
GDP/GTP exchange factor) encoded by a gene
GNOM [59, 63]. In plants with the gnom mutation, the
embryos cannot establish the polarity axis and die at
the earliest stage of development. The endocytosis
proceeds via clathrindependent pathway and is regu
lated by ROPGTPase Rab5 associated with the
endomembranes [62]. In addition, the vesicular trans
port of PINproteins is regulated by the factor
ARF/CAP/VAN3 acting as a possible antagonist of
the GNOM protein; this factor restricts the level of
PINproteins in the cell by directing them for degra
dation [55].
Vol. 59 No. 4 2012
 MECHANISMS AND PHYSIOLOGICAL ROLE OF POLARITY IN PLANTS
Thus, the polar flows of IAA in plant tissues depend
on the structure of actin microfilaments, the processes
of exo and endocytosis, and on the polar transport of
vesicles containing the auxin carrier proteins. The net
work of actin filaments together with ARF/GEF fac
tors establishes the polar arrangement of PINproteins
in the plasmalemma, thereby setting the direction of
polar auxin transport in the tissue (Fig. 2).
On the other hand, auxin itself can affect both the
dynamics of actin microfilaments and the vesicular
transport via a feedback mechanism. As the intracellu
lar content of IAA increases, the ratio of exo and
endocytosis is altered toward hindered internalization
of PINproteins, which increases the period of PIN
protein retention in the plasmalemma and, conse
quently, accelerates the auxin efflux from the cell [64].
Nick et al. [65] used transgenic Arabidopsis plants
overexpressing the actinbinding protein talin, which
led to the formation of thicker bundles of actin
microfilaments. These transgenic plants were charac
terized by low rates of IAA transport and by slow grav
itropic response. The treatment with exogenous IAA
restored the normal plant phenotype. In IAAtreated
plants the thick actin bundles disintegrated into thin
microfilaments, and the rate of IAA transport
increased.
It should be noted that the major part of auxin syn
thesized in mature leaves is carried over the plants
through the phloem rather than by virtue of polar
transport in the celltocell manner. The rate of
phloem transport of auxin (5–20 cm/h) is much
higher than the rate of its polar flows (0.5–1.5 cm/h).
The phloem is also the route for movement of IAA
conjugates. Apparently, the phloem flow of IAA and its
conjugates provide the basis for maintaining a certain
background level of free auxin and its bound forms in
plant organs and tissues.
The content of this hormone playing the central
role in regulation of morphogenesis is finely tuned by
means of PINproteins responsible for maintaining
the required auxin level in plant cells. The phloem
mediated and polar auxin transports are carried out
independently of each other. Nevertheless, there is
reason to believe that the IAA may enter for transloca
tion from the phloem pool into the system of polar
auxin transport; the possibility of the reverse transition
is not shown to date.
Polar Fluxes of Ca2+ Ions
In addition to basipetal polar transport of phyto
hormone IAA, active polar movement of Ca2+ ions in
plant tissues has been revealed. The polar calcium
fluxes move in acropetal direction under normal con
ditions but become transversely directed upon gravis
timulation, i.e., when the organ is reoriented from ver
tical to horizontal position [66].
The polar Ca2+ flux directed upward in gravistimu
lated maize coleoptiles was observed already in 10 min
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 59
509
after application of gravity stimulus. By contrast, the
flux of 14CIAA in the opposite direction appeared
only in 60 min after stimulation (table) [67].
The axial polar movement of Ca2+ was detected in
segments of sunflower hypocotyls [68], young fruits of
tomato and lettuce petioles [69, 70], maize coleoptiles
and pea internodes [71]. When 45Ca2+ was loaded onto
the basal end of the segment in our experiments, Ca2+
moved in the acropetal direction at an average velocity
of 19.0 ± 1.0 and 15.6 ± 0.8 mm/h in pea internodes
and maize coleoptiles, respectively. When the label was
loaded onto the apical end of the segment, the basipe
tal movement of Ca2+ ions was almost absent. The
radioactivity was detected mainly in the apical seg
ment, which directly contacted the agar block con
taining 45Ca2+ [67, 71]. Active transport of 45Ca2+ in
the acropetal direction was also observed in young
tomato fruits and lettuce petioles [69, 70]. The polar
Ca2+ fluxes were also detected with the use of calcium
selective electrodes in sunflower hypocotyls and maize
coleoptiles [68, 72].
It should be noted that the rate of polar acropetal
Ca2+ transport in plant axial organs is comparable to
the rate of counterdirected IAA movement. The
inhibitors of polar auxin transport (NPA and TIBA)
inhibited also the polar calcium transport [66, 67].
Therefore, there are grounds to believe that the polar
fluxes of Ca2+ and auxin are coupled.
Thus, there are two pathways of longdistance Ca2+
transport in plants. One of them is associated with the
transpiration flow, and the other represents the active
polar movement of this cation along the tissues. Active
polar fluxes of calcium ions are probably needed for
the formation of Ca2+ gradients in cells and tissues
with the polarized type of growth, as well as in tissues
with undeveloped vascular system, in the absence of
transpiration, and during tropic responses.
Plant morphogenesis is apparently initiated by the
formation of polar Ca2+ fluxes that establish the axis of
electrical polarity and affect the tissue distribution of
phytohormones (Fig. 2). The polar Ca2+ flow oriented
parallel to the gravity vector (or other polarizing fac
tor) might impose and adjust the directionality of
auxin flow, thus promoting the establishment of polar
ity axes, cell growth and differentiation.
MicroRNA
The term microRNA (miRNA) refers to endoge
nous short RNAs that do not encode proteins but sup
press gene expression by cleaving the transcripts of
these genes or by blocking the translation of mRNA
[73]. By this means, miRNAs control the expression of
almost half of the known genes coding for transcrip
tion factors. Plants synthesize hundreds of different
miRNAs that can move over symplast from cell to cell
and are likely to move in the phloem over long dis
tances.
No. 4 2012
510 MEDVEDEV
Distribution of 45Ca and 14CIAA during the gravitropic re
sponse of maize coleoptile segments [67]
45
Ca, 10 min 14CIAA, 60 min
Sample gravistimulation, gravistimulation,
% %
Upper segment part 165 100
Lower segment part 100 130
Note: A 100% level corresponds to the content of 45Ca in the
lower segment part and to the content of 14CIAA in the
upper part of the coleoptile segment.
MicroRNAs, like transcription factors, may also
serve as a “switch” of the programs of cell develop
ment. Once synthesis of certain miRNAs is induced
within the cell, it changes the fate of this cell line.
Therefore, the asymmetric (polarized) distribution of
microRNAs in plant organs and tissues would lead to
polarized suppression of the expression of target genes.
A wellstudied example is the repression by
miRNA165 and miRNA166 of PHABULOSA,
PHAVOLUTA and REVOLUTA genes encoding the
transcription factors of HDZIP family, which are
important for the establishment of dorsoventral sym
metry in the leaf [74]. Repression is achieved through
degradation of mRNA. In addition, DNA methyla
tion occurs in the genes PHABULOSA and
PHAVOLUTA. Another spectacular example of the
involvement of microRNAs in regulation of plant
development is the repression by miRNA172 of the
floral gene APETALA2 in primordia of the carpels and
stamens.
MicroRNAs are also involved in regulation of
embryogenesis and seed formation, in leaf and root
morphogenesis, proliferation of meristematic cells,
flower formation, and the hormonal signal transduc
tion [75, 76]
POLARITY IN GROWTH
AND MORPHOGENESIS
The concept of axial physiological gradient pro
posed by Child [77] turned out highly productive for
clarifying the role of polarity in regulation of growth
and differentiation. Child believed that physiological
activities of different parts of the organism are not uni
form and vary gradually in the direction of its morpho
logical axes. The physiological activity culminates at
one pole of the main morphological axis of the organ
ism and is minimal on the other pole; these poles are
separated by regions with intermediate activities.
Child supposed that physiological axial gradients pro
vide integrity and communications between different
organism parts and serve as the basis of differentiation.
Therefore, occasional failures in attempts to induce
morphogenesis in plant materials might reflect the fact
that experimental conditions do not always provide
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY
the adequate balance of endogenous phytohormones
in a specific tissue area. Under natural conditions such
balance depends primarily on physiological gradients
created during differentiation in vivo.
It should be pointed out that the plant development
depends not only on physiological gradients but also
on mechanical interactions between cells in growing
tissues [78]. Therefore, regulation of polar growth and
differentiation is based on metabolic gradients com
bined with mechanical signals and differential gene
expression.
Growth Gradients
Throughout the life cycle of almost all plant organ
isms, distinct gradients of growth rates can be
observed. For example, the growth of wheat leaves is
characterized by a gradient, with the growth rate
decreasing from leaf base to apex [79]. In bean hypo
cotyls the steep axial gradient of the growth rate was
discovered: the growth rates were high in segments
adjacent to the hypocotyl and gradually decreased
toward the base of the seedling [80]. Remarkably, the
segments with the highest initial growth rate showed
pronounced but transient responses to auxin applica
tion, whereas slowly growing basal segments exhibited
weaker but sustained enhancement of growth upon the
treatment with auxin. Similar growth rate gradients in
the axial direction were observed in pea epicotyls [81].
Differential growth rates and responses to IAA in
growing and fully expanded cells are apparently due to
the existing gradient in ion pump activities. In experi
ments with maize roots [82], the local elongation rates
were compared to the distribution of surface pH along
the roots. The most “acidic” surface pH was observed
at a distance of 4 mm from the apex; this root area was
characterized by the highest rate of cell extension.
The sequence of cell transitions to mitosis depends
on the size and position of cells with respect to the
organ main axis. The cell enters mitosis only after
reaching a certain size [83]. For example, for a pair of
sister cells in the root, the apical cell enters mitosis
earlier than the basal cell. This phenomenon stems
from the fact that the parent cell divides unequally, and
the apical daughter cell is always larger than the basal
cell.
Flowering Gradients
Many researchers were able to observe the so
called flowering gradients oriented parallel to the plant
main axis [84]. The presence of clearly evident flower
ing gradients was demonstrated with cultured explants
of tobacco, sampled from different plant parts [85].
When the explants were derived from the flower stalk
(peduncle), only flower buds were formed. If the
explants were obtained from the upper stem parts, they
formed both floral and vegetative buds. The explants
Vol. 59 No. 4 2012
 MECHANISMS AND PHYSIOLOGICAL ROLE OF POLARITY IN PLANTS
obtained from the lower stem internodes produced
only vegetative buds.
Differentiation of Vessels
Xylogenesis and formation of phloem elements are
characterized by the pronounced axial organization.
These processes depend largely on plant hormonal
status, Ca2+ concentration, and cytoskeleton [86]. It is
known that xylogenesis is inhibited by low levels of
external Ca2+, as well as by calmodulin inhibitors
(chlorpromazine, trifluoperazine) and Ca2+ channel
blockers (dihydropyridines, La3+) [87].
Auxin seems to play the leading role in the forma
tion of conducting vessels. Differentiation of vascular
bundles and other manifestations of polarity, including
cell division and cell elongation, are initiated and
guided by the flow of signals, with the auxin flow being
the most important [88]. New vascular tissues emerge
directly under developing buds and young leaves,
which are the source of IAA.
In studies of auxin action on differentiation of
phloem and xylem elements in turnip taproots, it was
found that the local application of IAA induced within
2 days the formation of conducting vessels in the
treated region [89]. By redirecting the routes of IAA
transport through the use of tissue incisions, it was
possible to modify the direction and density of vessels
formation in bean hypocotyls [90]. Thus, the auxin
produced in young leaves and transported into the
stem might be a signal for the formation of the vascular
system.
Since the IAAinduced differentiation of vascular
elements was inhibited by TIBA, we suppose that ini
tiation of morphogenesis requires not only a certain
auxin level but also its polar transport. It is the basipe
tal auxin transport that sets the vector for orientated
vascular development in the vertical direction. During
differentiation of the cambium (into the phloem or
xylem elements), the lateral concentration gradients
of IAA and sucrose were found essential [86, 91].
Remarkably, the phloem differentiation occurred in
the direction of lowering IAA/sucrose concentration
ratios, whereas the xylem was differentiated in the
direction of increasing IAA/sucrose ratios.
CONCLUSIONS
Polarity is an instrument through which the devel
oping organs and plant tissues are being mapped and
specific threedimensional structure of the organism is
created [92]. Owing to the polar organization, the
plants are able to orient themselves with respect to the
gravity vector and other vectorial cues and respond to
various stimuli. The main factor of the polar organiza
tion of growth, morphogenesis, and tropisms is the
polar transport of IAA [93], which is adjusted by the
polar fluxes of Ca2+ ions (Fig. 1). Almost all vectorial
environmental cues induce polar Ca2+ fluxes and pro
RUSSIAN JOURNAL OF PLANT PHYSIOLOGY Vol. 59
511
duce Ca2+ gradients in cells and tissues of the plant
organism. It is calcium fluxes that carry primary infor
mation about emerging polarization vector and ini
tiate the spatial pattern of metabolic activities and
morphogenesis [66, 67]. The earliest events include
ionic permeability changes of cell membranes result
ing in the specific pattern of electric currents. Accord
ing to a figurative expression of Goldsworthy [94], the
plant acquires its “electric compass” that allows the
spatial arrangement of growth and morphogenesis.
Further implementation of this positional information
leads to changes in the activity of ROPproteins,
cytoskeletal elements, and hormonal status, which
eventually results in differential gene expression and
commences the polar growth and differentiation.
ACKNOWLEDGMENTS
This work for supported by the Russian Foundation
for Basic Research, project no. 110400701a.
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