An Integrative Theory of
Plant Hormone Biology
Paul Pruitt, M.A. Biology, University of Pennsylvania 1984
This is the first version, Version I, of my ideas on Plant Hormones which was first written in 1986 and had not been previously published anywhere or posted on the Web until 06/06/2003. There are more recent versions available first written in 1995, 1999 and 2003. When the 1995 and 1999 versions were posted on the Internet, they received considerable comment, both positive and negative.
Knowledge in the field of plant hormones lacks unity. The five known hormones Auxin, Cytokinin, Gibberellin, Ethylene and Abscisic Acid appear to have a number of unrelated effects. My aim in this and a future paper is to put forth an integrative theory of plant hormones. I view each hormone as having a straight forward primary function that is crucial to the life of the plant. In order to survive, grow and reproduce, plants need three nutrients: Minerals, Water, and Sugar. Under some conditions, they can readily acquire the first two nutrients from the environment and manufacture the third. There is an "active" system for accomplishing these functions, which is run by two of the known hormones, Auxin (for Minerals) and Cytokinin (for Sugar) and a third about which we can only speculate. But under other conditions sufficient nutrients cannot easily be obtained. At these times, the plant must change its strategy in one or more of three ways: One, by "conservation", that is, by stopping or slowing growth or pruning unneeded older structures. Two, by "utilization", that is, by dipping into stored nutrients. Three, by "relocation", that is by changing growth patterns to improve the chances of later acquisition of nutrients. The other three hormones govern the "reserve" system which produces these changes in strategy. These hormones are Ethylene (for Minerals), Gibberellin (for Sugar), and Abscisic Acid (for Water).
Any theory of Plant Hormones needs to recognize the work of K. V. Thimann, F. Went, F. Abeles, F. Skoog, G. Avery, P. F. Wareing, P. Davies, P. W. Morgan, W. P. Jacobs, A. C. Leopold, A. W. Galston, R. Cleland, and F. Addicott. Forgive me for leaving out countless names of others who have made major contributions to the field. Special thanks goes to Mark Jacobs for getting me so interested in plants in the first place.
I'm not a professional scientist, and this "paper" is considered by most plant scientists to be pure speculation. Nevertheless I stand by what I write here because I believe it summarizes and draws valid conclusion from a large body of findings, producing a theory which is simple, cohesive and powerful. This "paper" suggests bold new directions for experiments and may have no other value than this. The use of "positive" and "negative" to describe the hormones, is not meant to put a value judgment on the hormones, but is instead meant to reflect the conditions of production and the effect of the hormone. In other words "positive," Plant Hormones are made under good growing conditions and produce further growth, whereas "negative" hormones are produced under bad growing conditions, and produce a cutting back on the size of the plant. They are simply names, however unfortunate some may consider them to be, that I currently use to describe the two sets of contrasting and complimentary Plant Hormones. At a later date the names can be changed, but they certainly are vivid.
There are four kinds of conditions under which nutrient acquisition cannot actively occur and the plant must rely on its reserve system. The first involves a change in the plant's environment such as shading, overcast, flooding, soil mineral depletion, or drought. Shading and overcast days stop or slow down photosynthesis and thus Sugar production. Soil mineral depletion and flooding make it difficult to acquire Minerals (flooding because this leaches Minerals from the surface layer of soil) (Sutcliffe, 1976).Drought quite obviously impedes the acquisition of Water. Under these conditions the plant must slow down its need for nutrients, dip into its reserves and alter parts of its structure in order to survive, grow and reproduce. Hence it must rely on elements of its reserve system.
A second condition requiring the reserve system is at night. During the night, the rate of photosynthesis is reduced and the plant has difficulty manufacturing Sugar. Also transpiration declines, reducing the uptake of Water and Minerals (because Minerals are dissolved in Water in the soil). During the day, the active system is at work and the plant, through transpiration and photosynthesis, acquires enough nutrients for both its day and night requirements. At night, the plant must rely more fully on its reserve system.
A third condition under which the reserve system must function is at the beginning of the life of a plant, when it is a seed. Before a seed is Watered, its Water supply must come completely from itself. After it is Watered but before the root and shoot stick out, the seed must rely totally on stored Minerals and Sugar to grow. The reserve system mobilizes these stored nutrients.
A fourth condition requiring the reserve system is at the end of the life of an annual plant, when it must use a large amount of nutrients over a short period of time to produce flowers, fruit and seeds. The plant cannot gain nutrients fast enough through active acquisition during this period. Hence it must rely on its reserve system to stop conventional growth and cannibalize its roots and shoots for their stored nutrients.
Active uptake of Minerals, Sugar and Water occurs during the middle part of the life of the plant between seed and senescence. During this period the plant needs to rely heavily on its active system to acquire a sufficient store of nutrients to be able later to make flowers and fruit and to set seed.
One can see that the plant needs two basic systems to handle its nutrient needs. It needs an active system to acquire or manufacture the nutrients from sources outside the plant when this is possible. It also needs a reserve system to conserve and utilize stored nutrients when active acquisition is blocked off. These two systems insure a smooth continuation of activities that contribute to survival, growth and reproduction. These two systems are governed by two sets of hormones.
How are these hormones mobilized? We can speculate that plants are similar to animals in that they maintain homeostatic levels of Sugar, Water and Minerals in their fluid system. Departure from these homeostatic levels produces signals that stimulate the plant to resolve the departure and return to homeostasis. Hence if its level of Minerals becomes low, the plant produces signals that stimulate acquisition or conservation of Minerals. If its Sugar level declines, there are signals that stimulate photosynthesis, produce more leaves, or release stored starch. Again if the plant becomes low in Water we can expect signals that stimulate the uptake of Water to return the plant to a homeostatic level. The signals in question are the release of one or another hormone.
Another important point is that the distribution of homeostatic deficiencies throughout the plant will seldom be even. For example there should be a relatively greater need for Minerals in the shoots, the point farthest removed from the mineral source at the roots. Hence the shoots are the place where the concentration of Minerals will most often fall below a homeostatic level. It follows that the signals for mineral deficiency are most likely to have their ultimate origin in the shoots. Additionally, Sugar deficiency should most often exist in the roots, because they are located at the greatest distance from the sites of photosynthesis. This suggests that the signals for Sugar deficiency are most likely to originate in the roots.
The points presented so far provide a basis for systematically linking specific hormones to the resource deficiencies they are hypothesized to correct.
The best known of hormones is Auxin or more specifically indole acetic acid (IAA). I would like to suggest that its role is to stimulate the plant to return to a normal homeostatic level of Minerals by-acquiring these nutrients from the environment. In short, IAA is an active mineral deficiency signal. The evidence for this position is as follows. IAA is made in response.-to mineral deficiency and not to mineral abundance (Wareinq and Phillips, 1981). It induces root growth in undifferentiated tissue thus stimulating mineral acquisition (Torrey, 1957). It is made in the shoots, particularly the shoot apex and young leaves where Minerals should be most deficient (Sembdner, et al., 1980). IAA peaks during the day (Jahardhan, et. al., 1973). It is also at its greatest level of concentration in the middle life of the plant between seed and senescence, when the root growth is most active and there is relatively little need for drawing on mineral stores.
Several other known effects of IAA suggest that this hormone serves to re-establish homeostatic levels of Minerals in the plant shoots. IAA induces undifferentiated tissue to make xylem (Jacobs, 1967), the highway along which Minerals travel from the roots to the shoots. This suggests that a shoot which is deficient in Minerals stimulates the cells below it to make xylem thus increasing the flow of Minerals to the shoot. Additionally IAA is known to cause hydrogen ion extrusion from cells (Reinhold, 1978), which is the first step to active uptake of mineral ions. If the shoot cells are low in Minerals and make IAA, this effect will cause them to extrude hydrogen ions and take up mineral ions, solving their problem. Finally IAA inhibits secondary buds from growing out (Snow, 1945; Palmer and Phillips, 1963). This should maximize the mineral concentration in the primary shoot apex and young leaves by cutting down on the mineral sinks of other shoots.
Another hormone is Cytokinin. Various items of evidence suggest that it is an active Sugar deficiency signal. Cytokinin promotes chlorophyll production (Beevers, et al., 1970), thus setting up the machinery for photosynthesis. It also promotes shoot formation (Skoog and miller, 1957), providing a locus for this machinery. It is made in the roots (van Staden and Smith, 1978), where we can expect the greatest Sugar deficiency.
Cytokinin also promotes the unloading of Sugar from phloem (Hayes and Patrick, 1985). Thus one can imagine that root cells which are low in Sugar would produce Cytokinin which would then cause the phloem in their vicinity to unload its Sugar, solving their Sugar deficiency. Cytokinin disinhibits secondary bud formation (Sachs and Thimann, 1967), producing more Sugar through the new leaves produced. It also inhibits the senescence of leaves (Pooviah and Leopold, 1973), thus preserving the Sugar producing organs of the plant.
Interestingly, just as Auxin induces xylem formation, Cytokinin induces phloem formation (Houck and Lamotte, 1977). This suggests that when root cells are low in Sugar, they induce the cells above them to be made into phloem, increasing the Sugar supply to the roots.
While Cytokinin peaks during the day, as might be expected of an active Sugar deficiency signal, it also peaks at night (Hewett and Wareing, 1973). The latter finding does not fit the theory, suggesting that the finding or some element of the theory needs further examination. All of these effects support a view of Cytokinin as adaptive Sugar deficiency signal. When the plant is low in Sugar, it makes Cytokinin in an attempt to exploit the environment to return the concentration of Sugar to a homeostatic level.
There is a great deal of evidence that Ethylene is a mineral reserve signal, conserving those Minerals that have been acquired and promoting the utilization of mineral stores. This hormone stops protein synthesis (Wareing and Phillips, 1981) and causes plants to lose proteins from their leaves (Abeles, 1967). Since proteins have heavy mineral content, these effects may help to reconcile mineral deficiencies. Ethylene also causes senescence of older leaves (Wareing and Phillips, 1981). With loss of leaves, there is a loss of mineral sinks; and if Minerals are withdrawn from the leaves during senescence, they can go along way toward solving mineral deficiencies. Ethylene also inhibits shoot growth (Reid and Wample, 1985), a development that should conserve Minerals. Ethylene is produced during flooding of plant cells (Imaseki, 1985), which suggests that excess ground Water which leaches Minerals from the soil may produce Ethylene. Ethylene is probably released during the germination of seeds (Esashi and Leopold, 1970) and may be especially important during the senescence of annual plants, though this is controversial (Nooden, 1980). All of these findings promote the identification of Ethylene as a signal for the conservation and utilization of the Minerals already absorbed by a plant.
Two of Ethylene's effects involve relocation of the root system. Ethylene broadens root cells (Burg and Burg, 1966) and initiates the growth of new roots (Zimmerman and Hitchcock, 1933). In doing so, it prepares the plant for later, improved mineral acquisition. That is, if existing roots do not take up enough Minerals, Ethylene encourages root relocation to explore new soil in search of this nutrient.
Two other effects of Ethylene suggest that it is a night hormone. The inhibiting effects of Ethylene on shoot growth (more specifically on stem elongation) are reduced in the presence of light (Wareing and Phillips, 1981). Also Ethylene levels are decreased by light (Goeschl, et al., 1967). These findings also mark Ethylene as an element of the reserve system.
Another piece of evidence provides a link between Ethylene and Auxin (IAA). Ethylene is produced by high levels of IAA (Rubinstein and Leopold, 1964). Since IAA results from a mineral deficiency, this means that Ethylene production can be ultimately traced back to Mineral deficiency, a key assumption of our theory.
The latter finding is particularly intriguing because it suggests that mineral deficiency produces a sequence of two signals. When the plant is low in Minerals, it first "tries" to solve its problem by releasing IAA, which induces an active mineral seeking strategy. If this strategy does not correct the deficit, the level of IAA continues to rise to the point where Ethylene is released, conserving Minerals and redeploying existing mineral stores. Thus Ethylene is a signal that is held in reserve in case of failures of IAA. It is possible that similar two-phase sequences are at work in response to Sugar and Water deficiencies.
Gibberellin (GA) fits well into the role of a Sugar reserve signal, which initiates activities designed to conserve Sugar and mobilizes reserve stores of this resource. GA causes the production of Alpha Amylase which dissolves stored starch (Varner, 1964). It antagonizes or stops root growth (Mitsuhashi-Kato, 1978) thus cutting down on Sugar deficits. GA levels go up in the dark when Sugar cannot be manufactured and down in the light (Brown, et al, 1975). GA delays senescence of leaves (Manos and Goldthwaite, 1975; Goldthwaite, 1972) thus maintaining those Sugar producing organs. GA is made in the roots (Barrington, 1975), where one would expect maximal Sugar deficiencies. Finally GA increases the flow of Sugar through the phloem (Hayes and Patrick, 1985) thus increasing the Sugar supply to deficient plant organs.
GA also causes lengthening of shoots (Engelke, at al, 1973). This suggests that plants which are manufacturing inadequate amounts of Sugar because of shading begin to produce GA, which lengthens their stems thereby relocating their leaves to a position where there is likely to be more sunlight. This prepares them for more effective photosynthesis.
GA levels also rise during germination (Webb, et al., 1973) and during the flowering of many plants (Zeevaart, 1983), implying that plants employ GA to mobilize their reserves in times of rapid growth. These effects reinforce the identification of GA as an element of the reserve system.
The last hormone, Abscisic Acid (ABA), can be reasonably construed as a Water reserve signal. ABA is released during dessication (Wain, 1975). It closes stomates (Wain 1975) thus preserving the Water that exists in the plant from evaporating. It causes dessication and senescence of older leaves (Marre, 1977), allowing their Water to flow into newer structures. ABA causes abscission of leaves (Addicott, 1964) thus removing Water sinks from the plant. It has been found to peak at night (Lecoq, et al., 1983; McMichael and Hanny, 1977), though the latter occurred only under Water stress. Although ABA is hypothesized to be important in the life of the seed before germination, this is still controversial (Black, 1983).
In summary, the hormones can be divided into active and reserve signals. The active signals acquire or manufacture nutrients. The reserve signals conserve existing nutrients, encourage the utilization of stored nutrients, and relocate parts of the plant for later, more effective nutrient acquisition.
IAA and Cytokinin appear to be the active signals for mineral and Sugar deficiencies respectively. When plants fall below their homeostatic levels of Minerals and Sugar, their first reaction is to release IAA and Cytokinin, which stimulates acquisition and manufacture of these resources. If this approach does not work, they turn to reserve strategies through the action of Ethylene and Gibberellin. Ethylene conserves Minerals, encourages mineral withdrawal from senescent leaves, and relocates parts of the root system. GA frees up Sugar stores and relocates the leaves for new and better efforts at photosynthesis.
The reserve signal for Water deficiency is ABA, which discourages Water evaporation, curbs Water use, and frees up Water from less effective organs. However the active signal that stimulates a plant to obtain Water is not yet apparent. A possible candidate for this status is Brassinosteroid, which causes plants to swell (Thompson, et al, 1982) as if taking up Water. Further research may possibly show that Brassinosteroid has other characteristics of an active Water deficiency signal such as suberization, stomate formation, vacuole formation, root or root hair formation, and the uptake of Water itself.
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Qualifications, Contact Information and Guestbook
My name is Paul Pruitt. I received a BA from Swarthmore College in 1984 where I studied under Mark Jacobs. My Bachelor's thesis was an examination of all aspects of Plant Senescence, including the role of hormones. I also received an MA from the University of Pennsylvania in 1986, where I studied plants under Scott Poethig among others. I have been studying the Plant Physiological Hormone Literature and thinking about Plant Hormones for 20 years. I'm currently an unemployed but experienced IT Support Analyst who has his own small file recovery and virtual Helpdesk business. The Website can be seen here. If you have any questions or comments send them to firstname.lastname@example.org.
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Barrington, E. J. W. Hormones. The New Encyclopaedia Britannica. Macropaedia v. 8, pp. 1074-88. Chicago: Encyclopaedia Britannica, Inc., 1975.
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