Auxin

Auxins (<small>plural of auxin</small> ) are a class of plant hormones (or plant-growth regulators) with some morphogen-like characteristics. Auxins play a cardinal role in coordination of many growth and behavioral processes in plant life cycles and are essential for plant body development. The Dutch biologist Frits Warmolt Went first described auxins and their role in plant growth in the 1920s.

Kenneth V. Thimann became the first to isolate one of these phytohormones and to determine its chemical structure as indole-3-acetic acid (IAA). Went and Thimann co-authored a book on plant hormones, Phytohormones, in 1937.

Overview

Auxins were the first of the major plant hormones to be discovered. They derive their name from the Greek word ( – 'to grow/increase'). Auxin is present in all parts of a plant, although in very different concentrations. The concentration in each position is crucial developmental information, so it is subject to tight regulation through both metabolism and transport. The result is the auxin creates "patterns" of auxin concentration maxima and minima in the plant body, which in turn guide further development of respective cells, and ultimately of the plant as a whole.

The (dynamic and environment responsive) pattern of auxin distribution within the plant is a key factor for plant growth, its reaction to its environment, and specifically for development of plant organs which generates the majority of auxin effects in intact plants, and is the most potent native auxin. And as native auxin, its equilibrium is controlled in many ways in plants, from synthesis, through possible conjugation to degradation of its molecules, always according to the requirements of the situation. Auxin can act in a heat sensitive manner in many situations, which will in turn effect a plant's phenotypic development.

Five naturally occurring (endogenous) auxins in plants include indole-3-acetic acid, 4-chloroindole-3-acetic acid, phenylacetic acid, indole-3-butyric acid, and indole-3-propionic acid. However, most of the knowledge described so far in auxin biology and as described in the sections which follow, apply basically to IAA; the other three endogenous auxins seems to have marginal importance for intact plants in natural environments. Alongside endogenous auxins, scientists and manufacturers have developed many synthetic compounds with auxinic activity.
Synthetic auxins fall into four classes: By covering various parts of the coleoptiles with a light-impermeable opaque cap, the Darwins discovered that light is detected by the coleoptile tip, but that bending occurs in the hypocotyl. However the seedlings showed no signs of development towards light if the tip was covered with an opaque cap, or if the tip was removed. The Darwins concluded that the tip of the coleoptile was responsible for sensing light, and proposed that a messenger is transmitted in a downward direction from the tip of the coleoptile, causing it to bend.

Peter Boysen Jensen

In 1910, Danish scientist Peter Boysen Jensen demonstrated that the phototropic stimulus in the oat coleoptile could propagate through an incision. These experiments were extended and published in greater detail in 1911 and 1913. He found that the tip could be cut off and put back on, and that a subsequent one-sided illumination was still able to produce a positive phototropic curvature in the basal part of the coleoptile. He demonstrated that the transmission could take place through a thin layer of gelatin separating the unilaterally illuminated tip from the shaded stump. By inserting a piece of mica he could block transmission in the illuminated and non-illuminated side of the tip, respectively, which allowed him to show that the transmission took place in the shaded part of the tip. Thus, the longitudinal half of the coleoptile that exhibits the greater rate of elongation during the phototropic curvature, was the tissue to receive the growth stimulus.

In 1911, Boysen Jensen concluded from his experimental results that the transmission of the phototropic stimulus was not a physical effect (for example due to a change in pressure) but serait dû à une migration de substance ou d'ions (was caused by the transport of a substance or of ions).

Perception

The best-characterized auxin receptors are the TIR1/ AFB family of F-box proteins. F-box proteins target other proteins for degradation via the ubiquitin degradation pathway. When TIR1/ AFB proteins bind to auxin, the auxin molecule acts as a 'molecular glue', a term coined by Ning Zheng, that allows these proteins to then bind to their targets (see below). The atomic structure of the perception mechanism of auxin by TIR1 was determined by X-ray crystallography.

Another auxin-binding protein, ABP1 is now often regarded as an auxin receptor (at the apoplast), but it is generally considered to have a much more minor role than the TIR1/AFB signaling pathway, and much less is known about ABP1 signaling.

The large number of Aux/IAA and ARF binding pairs possible, and their different distributions between cell types and across developmental age are thought to account for the astonishingly diverse responses that auxin produces.

In June 2018, it was demonstrated that plant tissues can respond to auxin in a TIR1-dependent manner extremely quickly (probably too quickly to be explained by changes in gene expression). This has led some scientists to suggest that there is an as yet unidentified TIR1-dependent auxin-signalling pathway that differs from the well-known transcriptional response.

On a cellular level

On the cellular level, auxin is essential for cell growth, affecting both cell division and cellular expansion. Auxin concentration level, together with other local factors, contributes to cell differentiation and specification of the cell fate.

Depending on the specific tissue, auxin may promote axial elongation (as in shoots), lateral expansion (as in root swelling), or iso-diametric expansion (as in fruit growth). In some cases (coleoptile growth), auxin-promoted cellular expansion occurs in the absence of cell division. In other cases, auxin-promoted cell division and cell expansion may be closely sequenced within the same tissue (root initiation, fruit growth). In a living plant, auxins and other plant hormones nearly always appear to interact to determine patterns of plant development.

Organ patterns

Growth and division of plant cells together result in the growth of tissue, and specific tissue growth contributes to the development of plant organs.

thumb|upright=1.35|Auxin diffuses along the shaded side of the plant, and causes cellulose in the cell wall to break, allowing turgor (water pressure) to expand the cell.

Growth of cells contributes to the plant's size, unevenly 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 originated because cells on one side grow faster than the cells on the other side of the organ. So, precise control of auxin distribution between different cells has paramount importance to the resulting form of plant growth and organization.

Auxin transport and the uneven distribution of auxin

To cause growth in the required domains, auxins must of necessity be active preferentially in them. Local auxin maxima can be formed by active biosynthesis in certain cells of tissues, for example via tryptophan-dependent pathways, but auxins are not synthesized in all cells (even if cells retain the potential ability to do so, only under specific conditions will auxin synthesis be activated in them). For that purpose, auxins have to be not only translocated toward those sites where they are needed but also they must have an established mechanism to detect those sites. Translocation is driven throughout the plant body, primarily from peaks of shoots to peaks of roots (from up to down).

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 short-distance, active transport exhibits some morphogenetic properties.

This process, polar auxin transport, is directional, very strictly regulated, and based in uneven distribution of auxin efflux carriers on the plasma membrane, which send auxins in the proper direction. While PIN-FORMED (PIN) proteins are vital in transporting auxin in a polar manner, the family of AUXIN1/LIKE-AUX1 (AUX/LAX) genes encodes for non-polar auxin influx carriers.

The regulation of PIN protein localisation in a cell determines the direction of auxin transport from cell, and concentrated effort of many cells creates peaks of auxin, or auxin maxima (regions having cells with higher auxin – a maximum). Proper and timely auxin maxima within developing roots and shoots are necessary to organise the development of the organ. PINs are regulated by multiple pathways, at both the transcriptional and the post-translational levels. PIN proteins can be phosphorylated by PINOID, which determines their apicobasal polarity and thereby the directionality of auxin fluxes. In addition, other AGC kinases, such as D6PK, phosphorylate and activate PIN transporters. AGC kinases, including PINOID and D6PK, target to the plasma membrane via binding to phospholipids. Upstream of D6PK, 3'-phosphoinositide dependent protein kinase 1 (PDK1) acts as a master regulator. PDK1 phosphorylates and activates D6PK at the basal side of plasma membrane, executing the activity of PIN-mediated polar auxin transport and subsequent plant development.

Surrounding auxin maxima are cells with low auxin troughs, or auxin minima. For example, in the Arabidopsis fruit, auxin minima have been shown to be important for its tissue development.

Auxin has a significant effect on spatial and temporal gene expressions during the growth of apical meristems. These interactions depend both on the concentration of Auxin as well as the spatial orientation during primordial positioning. Auxin relies on PIN1 which works as an auxin efflux carrier. PIN1 positioning upon membranes determines the directional flow of the hormone from higher to lower concentrations. Initiation of primordia in apical meristems is correlated to heightened auxin levels. They are upregulated via auxin influx.

Root growth and development

Auxins promote root initiation. Auxin induces both growth of pre-existing roots and root branching (lateral root initiation), and also adventitious root formation. As more native auxin is transported down the stem to the roots, the overall development of the roots is stimulated. If the source of auxin is removed, such as by trimming the tips of stems, the roots are less stimulated accordingly, and growth of stem is supported instead.

In horticulture, auxins, especially NAA and IBA, are commonly applied to stimulate root initiation when rooting 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, as a high concentration of auxin directly stimulates ethylene synthesis in axillary buds, causing inhibition of their growth and potentiation of apical dominance. When the apex of the plant is removed, the inhibitory effect is removed and the growth of lateral buds is enhanced. This is called decapitation, usually performed in tea plantations and hedge-making. Auxin is sent to the part of the plant facing away from the light, where it promotes cell elongation, thus causing the plant to bend towards the light.

Fruit growth and development

Auxin is required for fruit growth and development and delays fruit senescence. When seeds are removed from strawberries, fruit growth is stopped; exogenous auxin stimulates the growth in fruits with seeds removed. For fruit with unfertilized seeds, exogenous auxin results in parthenocarpy ("virgin-fruit" growth).

Fruits form abnormal morphologies when auxin transport is disturbed. 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 (PIN proteins).

Flowering

Auxin plays also a minor role in the initiation of flowering and development of reproductive organs. In low concentrations, it can delay the senescence of flowers. A number of plant mutants have been described that affect flowering and have deficiencies in either auxin synthesis or transport. In maize, one example is bif2 barren inflorescence2.

Ethylene biosynthesis

In low concentrations, auxin can inhibit ethylene formation and transport of precursor in plants; however, high concentrations can induce the synthesis of ethylene. Therefore, the high concentration can induce femaleness of flowers in some species.

Auxin inhibits abscission prior to the formation of the abscission layer, and thus inhibits senescence of leaves.

Synthetic auxins

In the course of research on auxin biology, many compounds with noticeable auxin activity were synthesized. Many of them had been found to have economical potential for human-controlled growth and development of plants in agronomy.

Auxins are toxic to plants in large concentrations; they are most toxic to dicots and less so to monocots. Because of this property, synthetic auxin herbicides, including 2,4-dichlorophenoxyacetic acid (2,4-D) and 2,4,5-trichlorophenoxyacetic acid (2,4,5-T), have been developed and used for weed control.

However, some exogenously synthesized auxins, especially 1-naphthaleneacetic acid (NAA) and indole-3-butyric acid (IBA), are also commonly applied to stimulate root growth when taking cuttings of plants or for different agricultural purposes such as the prevention of fruit drop in orchards.

Used in high doses, auxin stimulates the production of ethylene, also a native plant hormone. Excess ethylene can inhibit elongation growth, cause leaves to fall (abscission), and even kill the plant. Some synthetic auxins, such as 2,4-D and 2,4,5-T are marketed also as herbicides. Dicots, such as dandelions, are much more susceptible to auxins than monocots, such as grasses and cereal crops. So these synthetic auxins are valuable as synthetic herbicides. 2,4-D was the first widely used herbicide, and it is still in use. 2,4-D was first commercialized by the Sherwin-Williams company and saw use in the late 1940s. It is easy and inexpensive to manufacture.

Triclopyr (3,5,6-TPA), while known as an herbicide, has also been shown to increase the size of fruit in plants. At increased concentrations, the hormone can be lethal. Dosing down to the correct concentration has been shown to alter photosynthetic pathways. This hindrance to the plant causes a response that increases carbohydrate production, leading to larger fruit.

Herbicide manufacture

Synthetic auxins are used as a kind of herbicide and overdosing of auxins will interrupt plants' growth and lead to their death. The defoliant Agent Orange, used extensively by British forces in the Malayan Emergency and American forces in the Vietnam War, 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 U.S. Environmental Protection Agency 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, the use of 2,4,5-T products has been implicated in leukemia, miscarriages, birth defects, liver damage, and other diseases.