Polar auxin transport

Polar auxin transport is the regulated transport of the plant hormone auxin in plants. It is an active process, the hormone is transported in cell-to-cell manner and one of the main features of the transport is its directionality (polarity). The polar auxin transport has coordinative function in plant development, the following spatial auxin distribution underpins most of plant growth responses to its environment and plant growth and developmental changes in general.

Chemiosmotic model

Polar auxin transport (PAT) is directional and active flow of auxin molecules through the plant tissues. The flow of auxin molecules through the neighboring cells is driven by carriers (type of membrane transport protein) in the cell-to-cell fashion (from one cell to other cell and then to the next one) and the direction of the flow is determined by the localization of the carriers on the plasma membrane in the concerned cells.

The transport from cell to the neighboring one is achieved through relatively complex combination of several sub-processes. To explain the mechanism behind unique character of auxin transport through living cell files of the plant, the so-called chemiosmotic model was formulated.[1][2][3][4] The mechanism was first proposed in the seventies by Ruberry and Sheldrake[1][5] and this visionary[5] prediction was finally proven in the 21st century.

The mechanism below describes the process in which auxin is trapped in the cell by the so-called acid trap and how it can then leave the cell only by activity of specific carriers, which control the directionality of the flow from cells and generally the direction of auxin transport through the whole plant body.

Acid trap

See also: ion trapping
Passive diffusion on a cell membrane. However; in a case of auxins, only the non-dissociated portion of auxin molecules is able to cross the membrane

As weak acids, the protonation state of auxins is dictated by the pH of the environment; a strongly acidic environment inhibits the forward reaction (dissociation), whereas an alkaline environment strongly favors it (see Henderson-Hasselbach equation):

IAAH is in equilibrium with IAA− + H+, where IAAH = indole-3-acetic acid; IAA− = its conjugate base

The inside of cells (pH ~ 7) is less acidic than the outside (the apoplast; pH ~ 5.5). So outside the cell, significant portion (17%)[4] of the IAA molecules remain un-dissociated (proton-associated). This portion of auxin molecules is charge-neutral and therefore it is able to diffuse through the lipophilic lipid bilayer (lipid bilayer being constituent of cell membrane) into the cells.[4] Once through the bilayer in the cell, the molecules are now exposed to the more basic pH of the cell interior, and there they dissociate almost completely,[4] to give anionic IAA−, which being chemically polar are therefore unable to cross the lipid bilayer back again. So the auxin molecules are trapped inside the cell.[4]

Because the auxin can not leave the cell on its own anymore, the transport of anionic IAA out of the cell requires an active component in plasma membrane - some membrane transport protein. Membrane transport protein would allow the auxin molecules cross the membrane and leave so the cell. Two protein families: The PIN proteins and ABCB (PGP proteins) transporters are functioning as "auxin efflux carriers" and transport auxins from the cell.

Of those two, the PIN proteins are maintaining asymmetric localisation on plasma membrane: they are mostly located on the basipetal (i.e., root-ward) side of the cell and as consequence auxin is flowing from cells in the direction toward roots and root tips. The PIN proteins on membrane control directionality of the auxin flow.

Polarity of auxin export

Polarity is set up in the cell, as the efflux carriers are positioned asymmetrically on the plasma membrane. They are located normally only on the base of the plant cells (in direction towards the roots).

The location of PIN proteins is linked to the polarity of the transport. In most of the plant tissues, they are present on the rootward side of plant cells, meaning that they contribute to the general trend of moving IAA from the shoots to the roots.[6] But on some locations the positioning of PIN proteins is sensitive to environmental stimuli and the transporter proteins can be relocated to different side of cells in response to it. For example, the direction of the light source and gravity [7] triggers gravitropic and phototropic responses. This is also thought to be controlled by PIN proteins, as, when the stimuli reach the target cells, PIN proteins relocate to the sides and starts to pump auxin to one side of the root or stem respectively. PIN proteins fused with green fluorescent protein can visualize the localisation and its change of the PIN proteins on membranes. As auxin is pumped asymmetrically to the side of root of stem, it results in asymmetric growth (one side growths faster) and bending of the root or stem in response to the stimuli.

PIN proteins are so named because mutant plants lacking them cannot develop leaves (the formation of leaves is dependent on transported auxin), and so their seedling produces only a pin-like structure growing upwards.

Some experiments suggest that the asymmetrical development of efflux carrier protein requires the localized targeting of vesicles and the interaction with actin or the cytoskeleton. The process involves interaction of plasma membrane, plasma membrane proteins, the components of the cytoskeleton and cell wall.[8]

Effects of polar auxin transport

See also "Uneven distribution of auxin" and "Organization of the plant" in the main Auxin article

The polar auxin transport is required for generation of pattern of auxin gradients throughout the plant body.[5][9] Those gradients have development significances akin to the gradients of morphogens in animal bodies. They are necessary for development, growth and response of any plant organ[9] (such as cotyledons, leaves, roots, flowers or fruits) and response of plant to environmental stimuli known as tropisms.[10]

For example in process known as gravitropism, roots bend in response to gravity due to the regulated relocation of the plant hormone auxin inside the root tip.[10] That is, if a root is not oriented vertically, - so the bending downwards is actually developmentally required, gravity sensing mechanism inside root columella will reorient direction of auxin flow toward root down-side.[10] (Under normal situation, auxin flowing to columella by the centre of the root is redistributed to all sides from it and because it this is in the very tip of the root tip, the flow of auxin bend and flow backwards.[10] For visualisation it is sometimes described as reverse fountain, or umbrella shape flow). Mechanistically it is provided by the reorientation of the auxin efflux carriers described above. More precisely, after the gravity perception occurs, it is followed by reorientation of the PIN3 proteins on the plasma membranes in the cells of columella in such a way, that the PIN proteins are oriented down,[10] toward the gravity.

As a result one side of the root will be enriched by auxin more than the other one.[10] The increase in the concentration of auxin will inhibit cell expansion of the targeted cells (those on down side of the root), while cells on the other side of the root will continue to grow.[10] Because upper side of the root became to grow faster than the other one, it will eventually outgrowth around its position and turn downward. Therefore, the redistribution of auxin in the root can initiate differential growth in the elongation zone of the root, resulting in root curvature.[10]

Similar mechanisms are working in other tropic responses, such as phototropism.[10] The mechanisms were first described by the Cholodny-Went model, proposed in the 1920s by N. Cholodny and Frits Warmolt Went.[11]


Regulation

Inhibitors of the transport

In research, 1-N-Naphthylphthalamic acid (NPA) and 2,3,5-triiodobenzoic acid (TIBA) are used as specific inhibitors of the auxin efflux.[12]

Quercetin (a flavonol) and Genistein are naturally-occurring auxin transport inhibitors.[12]

9-Hydroxyfluorene-9-carboxylic acid (HFCA), TIBA, and trans-cinnamic acid (TCA) are also example of Polar Auxin Transport Inhibitors. They prevent the development of the bilateral growth of the plant embryo during the globular stage. All 3 inhibitors induce the formation of fused cotyledons in globular but not heart-shaped embryo.

Phosphorylation

Polar auxin transport can be regulated by reversible protein phosphorylation; protein kinases and protein phosphatases mediate the phosphorylation and dephosphorylation, respectively. A study suggests that phosphatase inhibition can alter the activities of acropetal and basipetal auxin transport.[7]

References

  1. ↑ 1.0 1.1 Rubery P and Sheldrake SH, P. H.; Sheldrake, A. R. (1974). "Carrier-mediated auxin transport". Planta 118 (2): 101–121. doi:10.1007/BF00388387.
  2. ↑ Raven, J (1975). "Transport of Indoleacetic-acid in plant-cells in relation to pH and electrical potential gradients, and its significance for Polar IAA Transport". New Phytologist 74 (163–172): 163. doi:10.1111/j.1469-8137.1975.tb02602.x.
  3. ↑ Goldsmith, M; Goldsmith T (1977). "Chemisomotic model for Polar Transport of Auxin". Plant Physiology 59: 90–90.
  4. ↑ 4.0 4.1 4.2 4.3 4.4 Zažímalová, E.; A. S. Murphy; H. Yang; K. Hoyerová; P. Hošek (2009). "Auxin Transporters--Why So Many?". Cold Spring Harbor Perspectives in Biology (Cold Spring Harbor Laboratory Press) 2 (3): a001552–a001552. doi:10.1101/cshperspect.a001552. ISSN 1943-0264.
  5. ↑ 5.0 5.1 5.2 Abel, S.; A. Theologis (2010). "Odyssey of Auxin". Cold Spring Harbor Perspectives in Biology 2 (10): a004572–a004572. doi:10.1101/cshperspect.a004572. ISSN 1943-0264.
  6. ↑ Variation in Expression and Protein Localization of the PIN Family of Auxin Efflux Facilitator Proteins in Flavonoid Mutants with Altered Auxin Transport in Arabidopsis thaliana - Peer et al., 10.1105/tpc.021501 - THE PLANT CELL
  7. ↑ 7.0 7.1 Gloria K Muday, Alison DeLong. (2001)Polar auxin transport:controlling where and how much. Trends in Plant Science 6(11):535-542
  8. ↑ Exploring the Cellular Basis of Polar Auxin Transport
  9. ↑ 9.0 9.1 Friml, Jiří (2003). "Auxin transport — shaping the plant". Current Opinion in Plant Biology 6 (1): 7–12. doi:10.1016/S1369526602000031. PMID 12495745.
  10. ↑ 10.0 10.1 10.2 10.3 10.4 10.5 10.6 10.7 10.8 Friml, Jiří; Wiśniewska, Justyna; Benková, Eva; Mendgen, Kurt; Palme, Klaus (2002). "Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis". Nature 415 (6873): 806–9. doi:10.1038/415806a. ISSN 0028-0836. PMID 11845211.
  11. ↑ Janick, Jules (2010). Horticultural Reviews. John Wiley & Sons. p. 235. ISBN 0470650532.
  12. ↑ 12.0 12.1 p.435 Plant Physiology Third Edition Taiz and Zeiger (2002)
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