Download Auxin and other signals on the move in plants Auxins are a class of

Auxin and other signals on the move in plants
Auxins are a class of plant growth substance and morphogens (often called phytohormone or plant
hormone). Auxins have an essential role in coordination of many growth and behavioral processes in the
plant life cycle. Auxins and their role in plant growth were first revealed by the Dutch scientist Frits Went.
Auxins derive their name from the Greek word αυξανω ("auxano" -- "I grow/increase"). They were
the first of the major plant hormones to be discovered. Their patterns of active transport through the plant
are complex. They typically act in concert with, or in opposition to other plant hormones. For example, the
ratio of auxin to cytokinin in certain plant tissues determines initiation of root versus shoot buds. Thus a
plant can (as a whole) react to external conditions and adjust to them, without requiring a nervous system.
On the molecular level, auxins have an aromatic ring and a carboxylic acid group (Taiz and Zeiger, 1998).
The most important member of the auxin family is indole-3-acetic acid (IAA). It generates the
majority of auxin effects in intact plants, and is the most potent native auxin. However, molecules of IAA are
chemically labile in aqueous solution, so IAA is not used commercially as a plant growth regulator.
1. Naturally-occurring auxins include 4-chloro-indoleacetic acid, phenylacetic acid (PAA) and indole3-butyric acid (IBA).
2. Synthetic auxin analogs include 1-naphthaleneacetic acid (NAA), 2,4-dichlorophenoxyacetic acid
(2,4-D), and others
Gallery of native auxins
indole-3-acetic acid
(IAA)
Indole-3-butyric acid
(IBA)
4-chloroindole-3-acetic acid (4CI-IAA)
2-phenylacetic acid
(PAA)
Gallery of synthetic auxins
2,4-Dichlorophenoxyacetic acid
(2,4-D)
α-Naphthalene acetic
acid (α-NAA)
2-Methoxy-3,6dichlorobenzoic
acid (dicamba)
4-Amino-3,5,6trichloropicolinic acid (tordon
or picloram)
α-(p-Chlorophenoxy)isobutyric
acid (PCIB, an antiauxin)
Auxins are often used to promote initiation of adventitious roots and are the active ingredient of the
commercial preparations used in horticulture to root stem cuttings. They can also be used to promote
uniform flowering, to promote fruit set, and to prevent premature fruit drop. Used in high doses, auxin
stimulates the production of ethylene. Excess ethylene can inhibit elongation growth, cause leaves to fall
(leaf abscission), and even kill the plant. Some synthetic auxins such as 2,4-D and 2,4,5trichlorophenoxyacetic acid (2,4,5-T) have been used as herbicides. Broad-leaf plants (dicots) such as
dandelions are much more susceptible to auxins than narrow-leaf plants (monocots) like grass and cereal
crops. These synthetic auxins were the active agents in Agent Orange, a defoliant used extensively by
American forces in the Vietnam War.
Hormonal activity:
Auxins coordinate development at all levels in plants, from the cellular level through organs and
ultimately the whole plant.
The plant cell wall is made up of cellulose, protein, and, in many cases, lignin. It is very firm and prevents
any sudden expansion of cell volume (and, without the contribution of auxins, any expansion at all).
Molecular mechanisms:
Auxins directly stimulate or inhibit the expression of specific genes.[2] Auxin induces transcription by
targeting for degradation members of the Aux/IAA family of transcriptional repressor proteins, The
degradation of the Aux/IAAs leads to the derepression of Auxin Respose Factors ARF-mediated
transcription. Aux/IAAs are targeted for degradation by ubiquitination, catalysed by an SCF-type ubiquitinprotein ligase. In 2005, it was demonstrated that the F-box protein TIR1, which is part of the ubiquitin ligase
complex SCFTIR1, is an auxin receptor. Upon binding of auxin, TIR1 recruits specific transcriptional
repressors (the Aux/IAA repressors) for ubiquitination by the SCF complex. This marking process leads to
the degradation of the repressors by the proteasome, alleviating repression and leading to expression of
specific genes in response to auxins (reviewed in Another protein called ABP1 (Auxin Binding Protein 1) is
a putative receptor, but its role is unclear. Electrophysiological experiments with protoplasts and anti-ABP1
antibodies suggest that ABP1 may have a function at the plasma membrane
On a cellular level:
On the cellular level, auxin is essential for cell growth, affecting both cell division and cellular
expansion. Depending on the specific tissue, auxin may promote axial elongation (as in shoots), lateral
expansion (as in root swelling), or isodiametric expansion (as in fruit growth). In some cases (coleoptile
growth) auxin-promoted cellular expansion occurs in the absence of cell division. In other cases, auxinpromoted cell division and cell expansion may be closely sequenced within the same tissue (root initiation,
fruit growth). In a living plant it appears that auxins and other plant hormones nearly always interact to
determine patterns of plant development. According to the acid growth hypothesis for auxin action, auxins
may directly stimulate the early phases of cell elongation by causing responsive cells to actively transport
hydrogen ions out of the cell, thus lowering the pH around cells. This acidification of the cell wall region
activates wall-loosening proteins known as expansins, which allow slippage of cellulose microfibrils in the
cell wall, making the cell wall less rigid. When the cell wall is loosened by the action of auxins, this nowless-rigid wall is expanded by cell turgor pressure, which presses against the cell wall.However, the acid
growth hypothesis does not by itself account for the increased synthesis and transport of cell wall
precursors and secretory activity in the Golgi system that accompany and sustain auxin-promoted cell
expansion.
Organ patterns:
Growth and division of plant cells together result in growth of tissue, and specific tissue growth
contributes to the development of plant organs. Growth of cells contributes to the plant's size, but uneven
localized growth produces bending, turning and directionalization of organs- for example, stems turning
toward light sources (phototropism), roots growing in response to gravity (gravitropism), and other tropisms
Organization of the plant:
As auxins contribute to organ shaping, they are also fundamentally required for proper
development of the plant itself. Without hormonal regulation and organization, plants would be merely
proliferating heaps of similar cells. Auxin employment begins in the embryo of the plant, where directional
distribution of auxin ushers in subsequent growth and development of primary growth poles, then forms
buds of future organs. Throughout the plant's life, auxin helps the plant maintain the polarity of growth and
recognize where it has its branches (or any organ) connected. An important principle of plant organization
based upon auxin distribution is apical dominance, which means that the auxin produced by the apical bud
(or growing tip) diffuses downwards and inhibits the development of ulterior lateral bud growth, which would
otherwise compete with the apical tip for light and nutrients. Removing the apical tip and its suppressive
hormone allows the lower dormant lateral buds to develop, and the buds between the leaf stalk and stem
produce new shoots which compete to become the lead growth. This behavior is used in pruning by
horticulturists.
Uneven distribution of auxin:
To cause growth in the required domains, it is necessary that auxins be active preferentially in them.
Auxins are not synthesized everywhere, but each cell retains the potential ability to do so, and only under
specific conditions will auxin synthesis be activated. For that purpose, not only do auxins have to be
translocated toward those sites where they are needed but there has to be an established mechanism to
detect those sites. Translocation is driven throughout the plant body primarily from peaks of shoots to
peaks of roots. For long distances, relocation occurs via the stream of fluid in phloem vessels, but, for
short-distance transport, a unique system of coordinated polar transport directly from cell to cell is
exploited. This process of polar auxin transport is directional and very strictly regulated. It is based in
uneven distribution of auxin efflux carriers on the plasma membrane, which send auxins in the proper
direction. A 2006 study showed plant-specific pin-formed (PIN) proteins are vital in transporting auxin.[4]
The regulation of PIN protein localisation in a cell determines the directional transport of auxin to
create the peaks of auxin, or auxin maxima. These auxin maxima help organise the development of the
root and shoot.[5].[6] . Surrounding auxin maxima are cells with low auxin troughs, or auxin minima. In the
Arabidopsis fruit auxin minima have been shown to be important for tissue development.
Locations:





In shoot (and root) meristematic tissue
In young leaves
In mature leaves in very tiny amounts
In mature root cells in even smaller amounts
Transported throughout the plant more prominently downward from the shoot apices
Effects:
Wounding response:
Auxin induces the formation and organization of phloem and xylem. When the plant is wounded, the auxin
may induce the Cell differentiation and regeneration of the vascular tissues.
Root growth and development:
Auxin induces new root formation by breaking root apical dominance induced by cytokinins. In horticulture,
auxins, especially NAA and IBA, are commonly applied to stimulate root growth when taking cuttings of
plants. However, high concentrations of auxin inhibit root elongation and instead enhance adventitious root
formation. Removal of the root tip can lead to inhibition of secondary root formation.
Apical dominance:
Auxin induces shoot apical dominance; the axillary buds are inhibited by auxin. When the apex of the plant
is removed, the inhibitory effect is removed and the growth of lateral buds is enhanced as a high
concentration of auxin directly stimulates ethylene synthesis in lateral buds causes inhibition of its growth
and potentiation of apical dominance.
Ethylene biosynthesis:
In low concentrations, auxin can inhibit ethylene formation and transport of precursor in plants; however,
high concentrations of auxin can induce the synthesis of ethylene. Therefore, the high concentration can
induce femaleness of flowers in some species.[citation needed]
Auxin inhibits abscission prior to formation of abscission layer and thus inhibits senescence of leaves.
Fruit growth and development:
Auxin delays fruit senescence.
Auxin is required for fruit growth and development. When seeds are removed from strawberries, fruit
growth is stopped; exogenous auxin stimulates the growth in seed removed fruits. For fruit with unfertilized
seeds, exogenous auxin results in parthenocarpy ("virgin-fruit" growth).
Auxin is important for the correct development of fruit. Fruits form abnormal morphologies when auxin
transport is disturbed.[8]. In Arabidopsis fruits auxin controls the release of seeds from the fruit (pod). The
valve margins are a specialised tissue in pods that regulates when pod will open (dehiscence). Auxin must
be removed from the valve margin cells to allow the valve margins to form. This process requires
modification of the auxin transporters.[7].
Flowering:
Auxin plays a minor role in the initiation of flowering. It can delay the senescence of flowers in low
concentrations.
Herbicide manufacture:
The defoliant Agent Orange was a mix of 2,4-D and 2,4,5-T. The compound 2,4-D is still in use and is
thought to be safe, but 2,4,5-T was more or less banned by the EPA in 1979. The dioxin TCDD is an
unavoidable contaminant produced in the manufacture of 2,4,5-T. As a result of the integral dioxin
contamination, 2,4,5-T has been implicated in leukaemia, miscarriages, birth defects, liver damage, and
other diseases. Agent Orange was sprayed in Vietnam as a defoliant to deny ground cover to the
Vietnamese army.
As multicellular organisms, plants, like animals, use endogenous signaling molecules to coordinate
their own physiology and development. To compensate for the absence of a cardiovascular system, plants
have evolved specialized transport pathways to distribute signals and nutrients. The main transport streams
include the xylem flow of the nutrients from the root to the shoot and the phloem flow of materials from the
photosynthetic active tissues. These long-distance transport processes are complemented by several
intercellular transport mechanisms (apoplastic, symplastic and transcellular transport). A prominent
example of transcellular flow is transport of the phytohormone auxin within tissues. The process is
mediated by influx and efflux carriers, whose polar localization in the plasma membrane determines the
directionality of the flow. This polar auxin transport generates auxin maxima and gradients within tissues
that are instrumental in the diverse regulation of various plant developmental processes, including
embryogenesis, organogenesis, vascular tissue formation and tropisms.
Introduction:
Plants differ from most animals in having a sessile lifestyles. They are thus limited in their capacity
to fight or rapidly escape from adverse environmental situations. To overcome these restrictions, plants
have evolved multiple mechanisms to flexibly adapt their growth to environmental conditions and nutrient
supplies. The most apparent examples of this life strategy include specific developmental responses to
various external stimuli, such as regulation of plant size and architecture in response to light availability
(shade avoidance, photomorphogenesis and phototropism). Plant hormones, which are small signaling
molecules, play a crucial role in regulating and coordinating plant growth and are involved in all
developmental processes, including directional growth responses (tropisms), control of plant architecture,
abiotic and biotic stress responses8,9 and flower and embryo development.
The phytohormone auxin plays a prominent role by acting as a versatile signal for spatial-temporal
coordination of development. Directional, intercellular auxin transport, a distribution mechanism unique to
auxin, generates differential distribution of auxin within plant tissues. The resulting auxin concentration
gradients, or localized areas with high auxin concentration (auxin maxima), provide positional information in
the course of many developmental processes. In plants, the distribution of substances can pose
complications because the absence of blood and lymphatic streams limits the effective distribution of
hormones, nutrients and metabolites. Therefore, plants rely on other transport mechanisms such as a
vascular system and intercellular transport pathways.
Two vascular networks, the phloem and the xylem, serve as the primary conduits for long-distance
transport but with opposite directions of flow (from and to the source tissues, respectively. Short-range
intercellular transport can be realized through three main mechanisms. (i) apoplastic transport through the
extracellular space, (ii) symplastic transport aided by the plasmodesmata, which are plant-specific
cytoplasmic tunnels and (iii) transcellular transport crossing both the intra- and intercellular space19 and
requiring repeated transport through plasma membranes. The goal of this review is to provide a general
overview of the different types of signaling molecule transport in plants, with a particular focus on the
directional, transcellular transport that is unique to the plant hormone auxin. This so-called ‘polar auxin
transport’ has been intensively studied for more than a century and is important in generating the
differential auxin distribution within tissues that is crucial to the regulation of many essential aspects of plant
development
Transported substances:
Water, nutrients, biomolecules and organisms such as viruses and fungi are all examples of cargos
that get transported throughout the plant by one or several different transport mechanisms. Mineral
nutrients, such as nitrogen, sulfur, phosphorus, magnesium, calcium and potassium, are taken up from the
soil as inorganic materials, assimilated into organic compounds and transported through the plant
depending on the balance between nutrient availability and the concentrations of the assimilated forms.
The transport of nutrients, and thus this balance, is regulated by both environmental (nutrients, carbon,
water availability) and internal (hormonal, metabolic, osmotic, energetic signals) cues mainly via regulation
of the activity or expression of specific transporters. Most macronutrients are used to manufacture amino
acids, proteins, nucleic acids, phospholipids, chlorophyll or the cell wall.
Phosphorus and magnesium, mainly in the form of Mg-ATP, have an important function in
bioenergetics. Potassium and calcium ions are crucial to maintaining the electrical potential of cellular
membranes. Potassium plays a specific role in guard cells, influencing the opening and closing of stomata
in response to external factors such as temperature, CO2 and light and helping to regulate the water
balance of the plant. Calcium, in plants as in other eukaryotes, is a major cytoplasmic secondary
messenger in many intracellular signaling pathways. Carbon is distributed mainly in the form of the
photosynthetic product sucrose, which is transported from the photosynthetic source tissues to sink tissues
(growing parts at the shoot and the root apices) where it is required for starch formation and storage during
fruit and seed development. Phytohormones, transcription factors and mRNA molecules are mostly locally
synthesized and transported as short-range signaling molecules to neighboring cells, but in some instances
they undergo vasculature- based long-distance transport as well. Pathogenic viruses and fungi have
adapted their infection strategies to hijack the plant transport pathways so as to efficiently spread through
plant tissues.
Types of transport:
Plants possess different transport systems that can be classified according to the distance and the
direction of transport. To assure that the substances are effectively distributed, higher plants combine a
long-distance transport system with a short-range cell-to-cell distribution network. Long-distance transport:
xylem and phloem. Xylem and phloem constitute the vasculature based transport systems. They both
consist of conductive elements that form continuous tubular columns. Xylem is made of tracheary
elements, which are dead, thick-walled cells that are depleted of their cellular content (including the
nucleus) and are perforated at both ends. The rigid composition of xylem also provides an essential
structural support, helping the plant to maintain its stature. Phloem, on the other hand, is formed by sieve
elements connected into a long sieve tube. In contrast to mature tracheary elements, sieve elements are
living cells but depleted of most of the cellular content.
In shoot stems of the model plant Arabidopsis thaliana, xylem and phloem are located in collateral
vascular bundles, with phloem at the periphery and xylem in the center. In Arabidopsis roots, xylem and
phloem are arranged in bilateral symmetry, with the xylem in a medial axis flanked by two phloem poles16.
Xylem transports and stores water, nutrients and hormones from the roots to the aboveground tissues (Fig.
1). The hormones transported by xylem include abscisic acid (ABA)25, cytokinins26 and strigolactones
newly identified hormones that regulate shoot branching5,6,27. Phloem distributes products of
photosynthesis (mainly carbohydrates), as well as proteins, mRNAs and hormones such as auxin28,
ABA25 and cytokinins, from the source tissues (photosynthetically active leaves and young buds) to sink
tissues.
Transport of signals through the phloem has been shown to be crucial for development and
defense against pathogens. A classical example of phloem’s developmental role is the transition from
vegetative development to flowering that is induced by day length–dependent photoperiodic stimuli
generated in leaves. One component of this so-called ‘florigen’ signal is the protein FLOWERING LOCUS
T, which is produced in the leaves and moves through the phloem to the shoot apex, where it activates the
flowering signaling pathway.
Plant hormones not only are transported through the vasculature but also have major effects on its
formation and differentiation. This is particularly true for auxin, which is a well-known player in determining
the complex pattern of vasculature in leaves, forming the vasculature connecting newly formed organs and
regenerating vasculature after wounding. During these processes, the initial auxin flow is reinforced through
a positive feedback regulation by auxin itself, which controls the throughput and directionality of the auxin
flow. This gradual canalization of auxin flow leads to the formation of auxin-transporting cell files (canals)
that demarcate the position of the future vascular strands. This self-organizing property of auxin transport is
referred to as the “auxin canalization model”. Other hormones are also involved in vasculature formation.
For instance, cytokinins act as negative regulators of xylem specification, whereas brassinosteroids
promote xylem differentiation.
Short-range transport. Membranes of plant cells are not in direct contact with each other because
of the presence of a cellulose-based cell wall. Thus, molecules have three possibilities for short-range
movement: (i) transport inside the cell wall, without entering the cell (apoplastic transport); (ii) direct
transport between the cytoplasm of two cells through the specialized, plant-specific structures known as
plasmodesmata (symplastic transport); and (iii) transcellular transport involving entering and exiting the
cells across the plasma membrane and crossing the apoplastic space between them.
Intercellular radial transport, combining the different types of cellto- cell transport pathways, often
contributes crucially to the loading of vascular stream. Water, nutrients and ions (boron, iron, magnesium,
nitrates and others) are absorbed from the soil by the root epidermis and are further transported through
the internal cell layers to the xylem. Apoplastic transport uses diffusion of transported molecules through
the cell wall all the way from the root surface to the endodermis cell sheet that surrounds the vascular
bundle. There, the apoplastic flow is limited by the Casparian strip, a massive deposit of suberin and/or
lignin, which are wax-like hydrophobic substances.
This structure creates a tight barrier that prevents the invasion of pathogens and restricts the
apoplastic flow of water and nutrients into and out from the vasculature. To reach the vasculature,
molecules have to cross the membranes of the endodermal cells and enter the symplasm. For example,
ABA, the drought stress hormone, as well as water and solutes move in the apoplast, but before reaching
the vascular flow, they enter the endodermis cells to pass the Casparian barrier. The apoplast is also the
main location for short-distance transport between the cells that secrete a signal and the target cells, where
the signal interacts typically with a cell surface–localized receptor, as is the case for hormones such as
brassinosteroids38 and cytokinins and for peptide-based signals such as the CLAVATA peptide that is
important for maintaining stem cell population at the shoot apex. Symplastic transport connects the
cytoplasm of two neighboring cells directly, through the plasmodesmata. Plasmodesmata are tunnels in the
plant cell wall that interconnect the cytoplasms of a group of cells and create symplastic domains that vary
in size during development.
The plasmodesmata-mediated transport of sugars, RNAs, peptides, signal proteins,
ribonucleoproteins, plant viruses and fungi is important in non-cell-autonomous signaling, signal relay,
defense against pathogens and distribution of nutrients. Symplastic transport is regulated by the exclusion
limit (‘aperture’) of the plasmodesmata pores, which control the passage of materials through
plasmodesmata based on molecular size. Some proteins targeted for this type of transport can specifically
adapt the exclusion limit to allow their own flow Passage through the plasmodesmata not only is a means
of transport but may also serve as a mechanism to regulate protein activity. An example is the
plasmodesmata-based movement of transcription factors such as SHORT-ROOT or CAPRICE, which are
involved in radial root and epidermis patterning, respectively. These proteins are cytosolic and inactive in
the cells in which they are produced, but after they have moved to neighboring cells through
plasmodesmata, they are targeted to the nucleus and become active in promoting transcription of
patterning factors. These observations imply that proteins can be modified by their passage through the
plasmodesmata, but the mechanism underlying this effect is unknown.
Transcellular transport is the movement of molecules from cell to cell without the use of direct
symplastic connections, which implies transport through plasma membranes by import-export mechanisms
such as membrane diffusion, secretion and receptor- or transporter-mediated systems. Such transport is
typically slower and more energetically demanding but allows more elaborate regulation and integration of
various signals at the level of each transporting cell. For example, nutrients have specific plasma
membrane transporters that are regulated by plant nutrient status and external cues. This regulation can
occur at several levels, such as transcription, degradation, trafficking or activity of the transporters. Signals
regulating the expression or activity of the transporters include nutrient availability, photosynthetic activity,
and the level of sucrose55,56 and cross-talk between nutrients. Some molecules such as boric acid, the
transported form of boron or auxin—use a transcellular transport mechanism. Boric acid, as a weak acid, is
radially transported by passive diffusion in the apoplast or by a transporter-mediated mechanism from the
root surface to the xylem.
There are two main transmembrane transport. mechanisms: import into epidermal, cortical or
endodermal cells, and export from endodermal, pericycle or xylem parenchyma cells into the xylem flow
(xylem loading). Polarly localized plasma membrane transporter proteins have been identified and found to
be involved in the cellular import and export of boric acid. Similarly, auxin transport uses a transcellular,
cell-to-cell pathway, characterized by influx and efflux transporters. This transport mechanism will be
discussed in detail because of its unique aspects and prominent implications for plant development.
Auxin transport and differential auxin distribution:
The principal naturally occurring form of auxin is indole-3-acetic acid (IAA), a weak acid derivative
of the amino acid tryptophan. Auxin is a small signaling molecule that acts as a versatile trigger in multiple
developmental processes including embryogenesis, organogenesis, vascular development and tropic
responses. Its distribution throughout the plant combines rapid, long-distance movement through the
phloem with a slow cell-to-cell transport that is highly regulated and occurs strictly in a given direction within
tissue. This transcellular type of transport is termed ‘polar auxin transport’. It is unique to auxin and was
discovered by Darwin while studying the phototropic growth responses of grasses to unidirectional light.
The actual chemical substance behind the growth-inducing (‘auxein’ in Greek) signal was isolated by Went
and Thimann several decades later.
The important recent discovery in the auxin field concerns the finding that in the course of many
auxin-dependent processes, the activity of auxin shows differential distribution between cells. Auxin activity
can be visualized indirectly in vivo by monitoring the activity of the synthetic auxin-responsive promoter
DR5. In theory, DR5 activity is proportional to the throughput of nuclear auxin signaling in a given cell and
should reflect levels of free, active auxin in the cell. Despite the obvious limitations of this approach,
measured DR5 activity has been shown to correlate well with auxin accumulation patterns (as inferred from
anti-IAA immunolocalization studies) during embryogenesis and organogenesis and in the root meristem.
In some instances, the differential auxin distribution can best be described in terms of local auxin
maxima, in which one or a small group of cells shows high auxin activity in sharp contrast with that of the
surrounding cells. Such local auxin accumulations or maxima can be seen during various organogenic
processes. For example, auxin accumulates in founder cells that will give rise to new organ primordia for
lateral roots, leaves or flowers, thus selecting these cells from the field of similar cells to undergo the fate
change. In other instances, such as in gynoecium development or root meristems, the auxin distribution
can be described in terms of a gradient, whereby the auxin concentration changes more gradually across
the tissue. Localized auxin minima can also regulate tissue patterning, as shown, for example, in fruit
development and seed dispersal.
Differential auxin accumulation is perceived and interpreted at the level of individual cells by the
nuclear auxin signaling pathway, which regulates gene expression and reprogramming of cell fates71.
Differential auxin distribution is essential for many developmental processes, and thus manipulation of
auxin distribution or cellular auxin signaling strongly disrupts the associated developmental process. One
important question concerns how this differential auxin distribution is generated and maintained. Both polar
auxin transport and local auxin biosynthesis contribute to differential auxin distribution. Two tryptophandependent auxin biosynthesis pathways, which are dependent on the YUCCA and TAA1 protein families,
are required for differential auxin distribution during some developmental processes.
Mutants defective in either of these pathways have aberrant DR5 activity patterns and related
developmental defects. Notably, different internal and external signals have been shown to modulate auxin
biosynthesis (at the level of transcription of the key enzymes) and polar auxin transport (at the level of
transcription, cell surface abundance and polar localization of transport components). As a result, transportdependent differential auxin distribution represents an additional level of regulation and signal integration in
auxin signaling.
The chemiosmotic model. Attempts to explain the mechanism underlying polar auxin transport
originally relied on biochemical and physiological studies that led to the formulation of the chemiosmotic
model in the 1970s. Auxin—IAA—is a weak acid, and its transporter-based transcellular pathway takes
advantage of the pH difference between the extracellular space and the cytoplasm that is generated by
plasma membrane H+-ATPases. The apoplast has a more acidic pH (5.5), in which IAA is partly protonated
and can diffuse passively through the plasma membrane into the cell. This passive influx is aided by the
action of auxin uptake carriers. In the more basic environment of the cytoplasm, IAA exists in its charged,
membrane-impermeable form and is trapped inside the cell, so that its transport out of the cell requires
auxin efflux carriers. Transport experiments using radioactively labeled auxin derivatives established that
auxin transport is directional (polar), with the main transport route running from the apex of the shoot
toward that of the root. To mechanistically explain this directionality, the chemiosmotic model postulated
that an asymmetric (polar) plasma membrane localization of the efflux carriers would determine the
direction of the intercellular auxin flow. This assumes that the polarity and polar targeting of auxin carriers
at the level of a single cell determines the directional transport of a signal between cells and, thus,
mediates the development of the whole tissue. The chemiosmotic hypothesis gained strong molecular
support after the auxin efflux carriers were identified and the importance of their polar subcellular
localization for the directionality of auxin flow was demonstrated.
The auxin transport proteins:
The chemiosmotic hypothesis originally postulated the existence of auxin influx and efflux carriers
in the absence of information about their molecular identity. Since then, largely thanks to the establishment
of Arabidopsis as a successful model organism for plant molecular genetics, the identity of the auxin
transporters has been revealed. These comprise (i) the AUX1/ LAX influx proteins, which mediate auxin
entry to the cell; (ii) the ABCB/PGP proteins, which mediate ATP-dependent auxin transport through the
plasma membrane; and (iii) the PIN exporters, which determine the directionality of auxin transport by
means of their polar subcellular localization.
The AUX1/LAX influx transporter protein family was identified through the isolation of the
Arabidopsis auxin1 (aux1) mutant. aux1 roots are resistant to the membraneimpermeable synthetic auxin
derivative 2,4- dichlorophenoxyacetic acid (2,4-D) and show agravitropic growth—both consequences of a
defect in cellular auxin uptake. The AUX1 gene codes for a protein homologous to amino acids permeases
and has been shown to mediate auxin import when heterologously expressed in Xenopus laevis oocytes.
AUX1 localizes to the plasma membrane of various cell types; notably, this includes asymmetric
localization at the upper side of young phloem (protophloem) cells of the root, where AUX1 presumably
unloads auxin from the phloem flow into the short-range transcellular transport pathway in the root
meristem.
In Arabidopsis, three LIKE AUX1 (LAX) proteins are present and also seem to function as auxin
influx carriers. For example, they act redundantly to regulate phyllotaxis86, and LAX3 has a unique role in
communication between the growing lateral root primordium and surrounding tissues. In summary, there is
compelling biochemical and genetic evidence that the AUX1/LAX proteins act as influx carriers and have
important roles in root growth, tropisms and organogenesis. Another class of transporters implicated in
auxin transport are the phosphoglycoproteins (PGPs), which are members of the B-type ATP binding
cassette (ABCB) transporter family. They were originally identified as proteins binding to the synthetic
inhibitors of auxin efflux. Some of these proteins—PGP1, PGP19 and PGP4—mediate auxin efflux and
show complex, multilevel functional interaction with other efflux transporters from the PIN family.
Combinations between pgp mutants and pin loss-of-function mutants indicate that these two types of auxin
exporters can act both synergistically and antagonistically in different developmental processes.
Although their functional relationship is far from clear, the PIN and PGP proteins probably comprise
two distinct auxin efflux mechanisms. At the polar domains where the PGP and PIN proteins colocalize and
interact, PGPs might act synergistically with PIN proteins in auxin efflux, possibly by regulating PIN stability
at plasma membrane microdomains. In addition, PGPs can also act at the nonpolar domains,
independently of the PIN proteins; in such a scenario, PGPs would mediate apolar auxin efflux and control
the amount of auxin available in PIN-expressing cells for the directional PIN-driven transport91. Thus,
complex interactions of directional PIN and ATP-dependent PGP-dependent transport systems at different
levels mediate directional auxin fluxes and ensure the fine regulation of the auxin distribution in many
developmental processes.
PIN proteins are crucial factors in determining the directionality of auxin flow. They have been
identified based on the auxin transport– related shoot and flower phenotypes of pin-formed1 (pin1) mutants
and the agravitropic root growth of pin2 mutants. The function of several Arabidopsis PIN proteins in
cellular auxin efflux has been demonstrated in tobacco BY-2 cultured cells, yeast and mammalian HeLa
cells88. Setting aside the PIN5, PIN6 and PIN8 subclade, whose function is unclear, the developmental
roles of the other five Arabidopsis PIN proteins are well documented and include actions during
embryogenesis, organogenesis, root meristem patterning, vascular tissue differentiation13 and tropic
responses. Notably, PIN proteins typically show asymmetric plasma membrane localization within cells, as
predicted by the chemiosmotic hypothesis for auxin efflux carriers. This polarity at the cellular level
correlates with and determines (at least in some instances) the directionality of the auxin flow within
tissues. Particularly important are changes in PIN subcellular polarity, because by this mechanism different
signals can redirect the auxin fluxes and trigger developmental reprogramming. For example, at early
stages of Arabidopsis embryo development, PIN7 is polarized at the upper side of suspensor cells and
mediates auxin flow to the young embryo, where auxin accumulates. However, at later stages of embryo
development, an as-yet-unknown signal causes polarization of PIN1 and PIN7 to the lower side of cells,
and thus auxin is redistributed from the embryo to the root pole where a new auxin maximum is established
.
PIN polarization and the resulting auxin root tip—translocates to the new bottom side of these
gravity-perceiving cells79,98. This PIN3 relocalization (presumably together with the redundant action of
coexpressed PIN4 and PIN7) redirects auxin flow toward the bottom side of the root, where auxin is further
transported, by a concerted action of AUX1 and PIN2, to the elongation zone85,99. Here auxin
accumulation inhibits growth, ultimately leading to the downward bending of the root. These examples of
PIN polarity switches demonstrate that this mechanism can be used to integrate diverse signals and to
trigger developmental changes by redirecting auxin fluxes.
Conclusions:
The transport mechanisms in higher plants, as exemplified by the model plant Arabidopsis, rely on
two main streams. First, the longdistance transport system depends mainly on the specialized conductive
tissue—the vasculature. The xylem serves as a means to transport water, nutrients and some hormones
from the root, whereas the phloem is used predominantly for the distribution of the photosynthetic products
and signals from the source tissues to the rest of the plant.
Second, short-distance cell-to-cell transport often complements vasculature-based translocation
and is used to load and unload substances from the vasculature as well as to distribute short-range signals
within tissues. Transported signals comprise signaling peptides, proteins such as transcription factors,
mRNAs and siRNAs that use an apoplastic, symplastic or transcellular transport mechanisms to move
through tissues and mediate a non-cell-autonomous signaling.
In addition, plant pathogens, including viruses, have adapted themselves to hijack existing
transport systems to efficiently infect plants. A special case of signal distribution is the cell-to-cell directional
movement of the phytohormone auxin, a versatile spatial-temporal signal. Polar auxin transport can
integrate various signals at the level of individual transporting cells and generate local auxin maxima and
gradients that are instrumental for many developmental processes. This unique signal-molecule transport
mechanism to a large extent underlies the remarkable developmental plasticity of plants that allows their
growth and architecture to adjust to changing environments.
Unraveling the mechanisms of transport and their associated regulation is of great economical and
ecological importance, for example to reduce the use of fertilizers or to engineer plants more suitable for
dry or other suboptimal growth conditions. However, there are still many open questions in our
understanding of transport processes in plants. The powerful approaches of molecular genetics have been
helpful, but they are limited by the potential lethality of mutations affecting essential transport processes
and by the extensive functional redundancy present in the genome. A combination of classical forward
genetics, chemical genomics and biochemical approaches may help to identify yet-undiscovered transport
components. Furthermore, transcriptome and metabolite profiling under various stress conditions have
hinted at extensive cross-talk between transport for different nutrients. The mechanisms and molecular
components of such cross-talk regulation are still largely unknown and will also be an important topic for
future studies.
References:
Helene S Robert and Jiri Friml (2009).Auxin and other signal on the move in plants. Nature Chemical
Biology.5 (5):325-332.
Alabadi, D., Blazquez,M.A., Carbonell,J.,Ferrandiz, C and Perezamador,M.A. (2009).Instructive role for
hormones in plant development. Int. J. Dev. Biol.53: (1597-1608).
Kusaka,N., Maisch,J., Nick, P., Hayashi, K.I and Nozaki, H. (2009).Manipulation of intercellular auxin in a
single cell by light with esterase-resistant caged auxins. ChemBioChem.10 :( 2195-2202).