How is auxin transported

The latter requires an integration of regulatory components, like kinases, chaperones, etc. The techniques to image kinase or transporter activities by usage of transport activity sensor and SPARK Separation of Phases-based Activity Reporter of Kinase assays and transporter-regulator interaction by using FRET are available and need to be transferred or optimized to the plant field Geisler, As for other disciplines, the identification of pharmacological inhibitors was extremely helpful for auxin transport research.

Since the work in the 's on maize coleoptile segments Hertel and Flory, and vesicles Hertel et al. Also overlooked is that NPA, like other phytotropins, is thought to bind to the same receptor, through which it performs its physiological responses Katekar and Geissler, ; Geissler et al.

This has led to speculation that the exporter might own a transceptor-like function Hossel et al. In the 's, different groups invested an enormous effort in characterizing the number, affinities and identities of putative plasma membrane-based NPA targets Michalke et al. The overall outcome as reviewed in Teale and Palme, revealed a very complex, partially contradicting picture with respect to the number and nature of the targets Teale and Palme, A route to the identification of an NPA target was provided by the isolation of the mutant allele pin-formed1 pin1 that resembles plants grown on NPA Okada et al.

Consecutively, the PIN1 gene was cloned and PIN1 was identified as a member of the major facilitator superfamily with a striking polar localization Galweiler et al. This correlation served as a quasi-accepted proof that PINs in general are NPA-sensitive auxin exporters, which was finally demonstrated in tobacco BY2 cells Petrasek et al.

For some time, a puzzling finding for the community was that PIN1 was inactive in heterologous non-plant systems, such as yeast or oocytes, shedding some doubt on its direct function as a transporter. However, also this missing detail was solved by the finding that PIN1-mediated transport is strictly dependent on phosphorylation, which was provided either by AGC kinase co-expression or phospho-mimicry Zourelidou et al. Using chemical-genetic screens, the NPA analog, BUM 2-[4- diethylamino hydroxybenzoyl]benzoic acid , was identified and shown to have an IC 50 value that is roughly a factor 30 lower Kim et al.

TWD1 seems to own a second function on auxin transport that involves bundling of the actin cytoskeleton Zhu and Geisler, ; Zhu et al. Interestingly, both the epidermal twisting in abcb1 abcb19 and twd1 can be partially rescued by NPA treatments Wang et al. Another promising outcome of the initial NPA-affinity chromatography Murphy et al. Grand Challenges : Overall it seems that 60 years after its first description, we now have a slightly better understanding of NPA action and it is good to see that initial predictions that NPA interferes primarily with the efflux complex seem to hold true.

It is now clear that the path to understand NPA was heavily complicated by the fact that there are multiple NPA targets in plants, each with different binding affinities that partially interact with each other.

On top it was shown that some of these interactions, such as between PINs and ABCBs, can influence the binding affinities of these complexes Blakeslee et al. Another level of complication is caused by the fact that NPA seems to interfere with transporter phosphorylation. Finally, there are reports that NPA might directly interfere with actin bundling in an action that is independent of TWD1 Dhonukshe et al. It is remarkable that our understanding of the mechanism of such an important research tool used in so many labs around the world is still incomplete.

At the next level, a systematic in planta dissection of NPA-sensitivities of auxin transport complexes must be achieved using suitable approaches, such as quantitative proximity ligation assays PLA; Teale et al. Having the protein targets in hand, would allow for the development of specific efflux inhibitors that are more selective toward a certain transporter class. Moreover, it will be essential to completely understand the overlapping pin-formed phenotype that is thought to be caused by genetic pin1, pinoid or pharmacological inhibition NPA, BUM of PAT that has branded the PIN subfamily.

Despite our progress, it is still noteworthy that until today a plausible explanation for the inflorescence defects in pin1 is still missing, especially in light of the fact that auxin levels in these tissues are not different to wild-type Jones et al.

Furthermore, one should not forget that growth on NPA or BUM likely leads to a saturated inhibition of all NPA targets in the plant making pin-formed inflorescences most-likely a pleiotropic phenotype. That PIN1 was recently found to form complexes with multiple proteins, including other PIN isoforms, supports this overall concept Blakeslee et al. Finally, a continuously open question is the existence of a native NPA analog, which was originally assigned to flavonol derivates based on their ability to compete out NPA in binding assays and their ability to inhibit PAT Murphy et al.

For a while these were discarded Peer and Murphy, ; Teale and Palme, , however, recent work showing that they inhibit PIN transport by dimerization in analogy to NPA might place them back on the table Teale et al.

However, in this respect it might be important to recall that this effect like the one for NPA could be also simply caused by inhibition of kinases involved in PIN phosphorylation that would lead to a similar result. These ideas persist today in the community and are thus very difficult to revise. This created an atmosphere that was built on doubt and ignorance, and did not promote scientific progress.

In that respect, I would like to suggest a reset and that we should become again interested in differences between auxin transporters with respect to their polarity, their mode of energization, plasma membrane stability or NPA sensitivity.

We should see differences in auxin transport data more like a challenge than a flaw, which is in general probably a good mindset. Throughout this perspective article, I have summarized and critically evaluated current knowledge as well as the many inconsistencies in the field.

I have considered what could be done if energies and resources were fostered. In my eyes, the perspectives are clear but will require a better and more neutral, meaning a less self-centered, approach. Such a change in attitude might represent the biggest future challenge for the community.

But it is worth trying as it has the potential to assist us to refocus on the essentials, which is after all the beauty of auxin transport.

As a positive, it will help us to regain lost trust inside the plant community. In addition to the grand challenges for basic research of auxin transport, we urgently need to better integrate with the applied sciences.

Considering the important roles that auxin transport plays for plant development, we should keep an eye to the future of life on the planet. This focus might include the production of food, forage, fiber, fuel and pharmaceuticals as well as ecosystem services. We need to apply our basic research to societal questions, like feeding our children's children, environmental questions, like growing plants in climates where we already see changes that negatively impact quantity and quality of plant products and species diversity.

The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers.

Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. The author would like to deeply thank Wendy Ann Peer and Angus Murphy for their long-lasting collaboration and friendship and the many helpful comments on the manuscript.

This retro-perspective article is dedicated to Rainer Hertel, one of the pioneers of auxin transport research. Abas, L. Naphthylphthalamic acid associates with and inhibits PIN auxin transporters. Adamowski, M. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27, 20— Anfang, M. Transport mechanisms of plant hormones. Plant Biol. Bailly, A. The twisted Dwarf's ABC: how immunophilins regulate auxin transport. Plant Signal Behav.

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Garbers, C. A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis. EMBO J. Geisler, M. Seeing is better than believing: visualization of membrane transport in plants. A critical view on ABC transporters and their interacting partners in auxin transport.

Plant Cell Physiol. Acta , 52— Tete-a-tete: the function of FKBPs in plant development. Master and servant: regulation of auxin transporters by FKBPs and cyclophilins. FEBS Lett. Auxin transport during root gravitropism: transporters and techniques. Geissler, A. Growth and gravireaction of maize roots treated with a phytotropin. Goldsmith, M. In cases when assays have been established, often no experiments using NPA were reported Petrasek et al.

Plant microsomes have, however, been measured as binding NPA with more than one distinct K m , and it is the weaker affinity binding events which match well with the concentrations of NPA that inhibit auxin transport and could potentially be ascribed to PIN binding activity Michalke et al.

It should, however, be noted that NPA binds to microsomes prepared from pin1 Arabidopsis plants with only slightly less affinity than to those prepared from wild-type plants, though endogenous NPA-like compounds were present in this assay, as were other plasma membrane-localised PINs Rojas-Pierce et al.

As it is a weak aromatic acid, protonated TIBA is thought to diffuse into cells in a similar way to IAA, though with fold greater permeability under physiological conditions Depta et al.

Whether these differences are able to reconcile the experiments with the observation that 2,4-D is not a substrate for the efflux carrier is unclear Delbarre et al. In fact, the truth is likely to be a good deal more complicated than IAA and TIBA competing for a single binding site on a single carrier.

A two site model for polar IAA and TIBA transport was subsequently proposed along with suggested compromises necessary to reconcile it with the binding data of Ray et al. Ray et al.

In it, TIBA and IAA bind to separate, but functionally related sites on the efflux transporter, and the transport of either is inhibited when both are bound simultaneously. This section does not aim to give a broad overview of the role of flavonols in the regulation of auxin transport.

For this, many good summaries are already available Rubery, ; Peer and Murphy, ; Buer et al. Instead, we aim to highlight some pressing questions raised by studies of the endogenous regulation of polar auxin transport. Why should plants have evolved multiple protein structures able to bind, sometimes with high affinity, a synthetic chemical such as NPA to which they have never been exposed?

This question was answered by a study in the late s which demonstrated that the ability of different flavonols to inhibit vesicular auxin efflux correlates with the ability of those compounds to displace NPA from the same membrane preparations Jacobs and Rubery, Flavonols form a class of compounds that belong to the wider family of flavonoids, which also includes flavanols, flavones, and anthocyanins. Though structurally similar, there is sufficient opportunity for modification to the basic backbone of three benzene rings to give the more than flavonoids that have been characterized.

Flavonols can be distinguished from the other major classes of flavonoid compound by their distinct patterns of hydroxylation and oxidation of carbons on all three of their benzene rings Taylor and Grotewold, The series of experiments that confirmed the flavonols as endogenous regulators of auxin transport were conducted on a genotype known as transparent testa4 tt4.

This plant lacks chalcone synthase: the first enzyme that is dedicated to flavonoid biosynthesis Shirley et al. Endogenous flavonols not only inhibit the rootward transport of auxin, but also affect the PIN2-dependent shootward reflux of auxin in the outside cell layers of the root meristematic zone Buer and Muday, It is, however, unclear whether the regulation of shootward auxin flux is via the effect of endogenous flavonols on the efficiency of PIN mediated auxin transport Rojas-Pierce et al.

ABCB19 was identified in a mutant screen as the locus that confers sensitivity to gravacin Rojas-Pierce et al. Here we come across a counterintuitive aspect of polar auxin transport regulation: inhibiting auxin flux can lead to an increase in sensitivity to gravity, whereas increasing flux causes a decrease Noh et al.

This has been explained by different treatments or genotypes having relatively different effects on the strength of shootward and rootward auxin transport systems. Here, an attenuation of the gravitropic response would be caused by relatively strong rootward flux in the absence of endogenous flavonols. The endogenous function of flavonols with respect to the regulation of auxin transport is likely to be more nuanced than is the exogenous application of NPA, with different flavonols and flavonol glycones being localized to different parts of the plant and playing different physiological and developmental roles Kuhn et al.

This view is supported by a series of experiments on tt flavonol-deficient mutants that showed a range of different abilities to transport auxin and displayed associated phenotypes such as gravitropic and lateral rooting defects Buer et al.

Though the ability to compete for NPA binding and the ability to inhibit auxin transport were generally correlated among a range of flavonols, there were notable outliers, for example morin, which associated readily with NPA binding sites but did not inhibit auxin transport Jacobs and Rubery, PIN proteins are also likely to have different sensitivities to any given flavonol.

For example, in pin2 plants, the PIN1 expression domain expands into the epidermis where it mediates shootward auxin flux Santelia et al. Transport and environmental regulation of flavonol availability undoubtedly occur, but their overall significance still remains unclear Thompson et al.

For example, a transient increase in flavonoid concentration which occurs two hours after a gravity stimulus in wild-type roots plays a role in the gravitropic response, however it is unclear to what extent this response is tuned to a specific flavonol-PIN interaction Buer and Muday, Although protein phosphorylation stimulates the activity of auxin efflux carriers Delbarre et al.

However, assigning the activity of specific kinases to either the stimulation or inhibition of NPA-sensitive auxin efflux has not been straightforward. This is probably because various kinases participate in regulatory circuits that both enhance and repress auxin efflux, indicating regulation is multi-level and complicated Bernasconi, ; Delbarre et al.

In some cases, kinase, phosphatase, and protein targets are known. For example, two independent lines of enquiry, each beginning with the characterization of phenotypes which resembled either NPA-treated Bennett et al. It was identified after a screen that measured the sensitivity of mutant plants in a root growth assay; as roots grow through agar, after touching the bottom of a horizontal petri dish, they tend to grow in an inward spiral.

This growth response is specific: rcn1 plants respond as wild-type plants to other polar auxin transport inhibitors such as TIBA Garbers et al. This is unlikely as shootward auxin transport at the root tip is inhibited by NPA to the same extent in rcn1 and wild-type plants Rashotte et al.

However, of great interest is a complementary experiment that demonstrated that NPA does not inhibit transport in the opposite direction in rcn1 , especially as a phosphatase inhibitor had the same effects Rashotte et al.

These data suggest different mechanisms regulate shootward and rootward auxin flux in the root apical meristem and that RCN1 plays a different role in each. Another interesting aspect is that here, NPA may not be considered as simply a synthetic analog of the flavonols. Not only did quercetin prove to be a more effective inhibitor of PID activity than NPA, as measured by levels of PID autophosphorylation, but it showed an increased, rather than a decreased affinity for ABCB1 when a phosphomimetic glutamic acid was substituted at the PID substrate site Henrichs et al.

This work represents an exciting direction of enquiry that could uncover the molecular basis for different regulatory effects between NPA and the flavonols on polar auxin transport. A careful genetic dissection of the activity of flavonols in rol also revealed a role for protein phosphorylation in flavonol-mediated polar auxin transport inhibition Kuhn et al.

Here, data are consistent with a hypothesis that the observed apical localisation of PIN2 in root cortex cells of rol plants is caused by the presence of unusual flavonols. Furthermore, the results from a gravitropic response assay have been used to make a compelling argument that PID kinase activity is decreased by the activity of flavonols Kuhn et al.

Further investigations of the key players behind these phenotypic relationships promise new insights into the mechanisms of polar auxin transport regulation. NPA has given us rare glimpses into the inner workings of the auxin efflux carrier complex and its regulatory proteins but now stands at a crossroads.

Although it has brought our understanding of polar auxin transport forward a long way, at the heart of this research and commentary there remains contradiction and controversy. For example, the chemiosmotic hypothesis, the accepted model that provides the foundation for our understanding of polar auxin transport, requires transporters energized by a pH gradient across the plasma membrane.

However, the proteins that bind the most prominent transport inhibitors, and therefore must be placed at the centre of any transport model, belong to a protein family that depends on the hydrolysis of ATP for substrate efflux.

The usefulness of NPA depends on its ability to precisely dissect either the auxin transport mechanism directly, or the signaling processes which control it.

At best, our clearest understanding points to a simultaneous influence over transport and control. However, are exisiting inhibitors Fig. Wherever NPA takes us in the future, it is clear that the journey will need standardized, robust in vitro auxin efflux assays if results are to be compared effectively, and existing physiological data will need to be put into this molecular context as it continues to emerge. Auxin and some inhibitors of its polar transport, with their relevant analogs.

Pink shading and a dotted line indicate compounds that do not occur naturally in plants. Blue shading and a solid line indicate auxin transport inhibitors. Thanks also go to Rainer Hertel for valuable discussions. The authors declare that no competing interests exist.

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Auxin transport regulation. Auxin transport routes during embryogenesis. Auxin and postembryonic root and shoot development.

Auxin in vascular tissue development. Auxin routes in tropisms. Article Navigation. This site. Google Scholar. Author and article information. Online Issn: Development 16 : — Cite Icon Cite. Table 1. Selected auxin carriers with established developmental roles. Role in development. Key references. Auxin influx carrier AtAUX1 Root gravitropism, lateral root formation, phloem loading in leaves and unloading in roots, root hair development, phyllotaxis, hypocotyl phototropism Bainbridge et al.

View Large. Transport of various compounds including auxin towards the tip of a particular organ stem or root. Cell division in a layer of cells that occurs perpendicular to the plane of the cell layer.

Cell division in a layer of cells that occurs parallel to the plane of the cell layer. The first root that develops from the embryonic root of a plant embryo,the radicle.

The central part of the root or stem that contains the vascular tissue. Box 2. Physiology-based models of auxin transport across the plasma membrane A model for the mechanism that underlies the directionality of cell-to-cell auxin transport was proposed simultaneously by Rubery and Sheldrake Rubery and Sheldrake, and Raven Raven, , and is known as the chemiosmotic polar diffusion model Goldsmith, View large Download slide.

Box 3. Tracking auxin distribution and transport in plants View large Download slide. Box 4. Intracellular trafficking of auxin transporters View large Download slide. Abas, L. Bainbridge, K. Bailly, A. Bell, C. Benjamins, R. Bennett, M. Blakeslee, J. Blilou, I. Carraro, N. Chen, L. Chen, R. Cho, M. Christensen, S. Darwin, C. Delbarre, A. Dello Ioio, R. Dharmasiri, N. Dharmasiri, S. Dhonukshe, P.

Dubrovsky, J. Friml, J. Geisler, M. Geldner, N. Goldsmith, M. Hamann, T. Hardtke, C. Heisler, M. Hochholdinger, F. Jahrmann, T. Jaillais, Y. Jones, A. Kamada, M. Kepinski, S. Kleine-Vehn, J. Laxmi, A. Lewis, D. Li, J. Lin, R. Ljung, K. Luschnig, C. Malenica, N. Mancuso, S. Marchant, A. Men, S. Michniewicz, M. Mravec, J. Multani, D. Murphy, A. Nagashima, A. Ni, W. Noh, B. Okada, K. Oliveros-Valenzuela, M. Paciorek, T.

Parry, G. Raven, J. Reinhardt, D. Rojas-Pierce, M. Roman, G. Rubery, P. Sabatini, S. Sachs, T. Santelia, D. Sauer, M. Scarpella, E. Schnabel, E. Schrader, J. Sorefan, K. Stiefel, V. Stone, B. Swarup, R. Swarup, K. Terasaka, K. Titapiwatanakun, B. Ulmasov, T. Utsuno, K. Vanneste, S. Vieten, A. Verrier, P. Weijers, D. Went, F. Willemsen, V. Wu, G. Xu, M. Yang, H.

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