Control circuitry and individuality
The genetic analysis of flowering time in arabidopsis will probably provide a paradigm for the genetic control circuitry that underpins other timing processes, such as breakage of bud and seed dormancy, in plant development. Although the precise molecular details are still being uncovered, some very broad outlines of control circuitry are now indicated (Simpson and Dean, 2002). Robust control circuits involve both feed-forward and feedback regulation, and obvious signals that attempt to propel the system forward or hold it back are obviously present in the flowering time circuitry. Integration of different signals is achieved, it is thought, by protein/protein interaction from different input signals on the promoters of integrator genes. Redundancy in the circuitry is also evident, providing for fail-safe mechanisms. Plasticity in flowering time results from quantitative variations in overlapping pathways. Further investigation may reveal the extent to which controls consist of modular groups of proteins that can be changed en bloc as it were and which overlap with each other providing reliability (Hartwell et al., 1999). Hierarchical organization of modularity has already been detailed in metabolic networks (Ravasz et al., 2002). However, these basic elements in control circuitry are what might be expected to control plasticity.
While genetics is a powerful investigative tool, we are not dealing with bacteria in which mutation affects only the cell in which it is expressed. Instead, the individual plant is a complex, multicellular and multi-tissue organism in which development is continuous and in which communication is paramount. Flowering time, an aspect of plasticity and behaviour, is a composite response involving all parts of the organism, including its life cycle. Mutations, the normal means of identifying relevant genes that modify any character, are often present throughout the whole life cycle. Knock-on consequences from some mutations may then only indirectly affect later processes such as flowering time. Intelligent behaviour is a holistic quantity reflecting in turn the whole organism, but some of the circuit control indicated above for flowering should be present at a whole-plant level.
The problems of resource gathering and predation for a sessile organism seem to be the major evolutionary pressures that have generated minimal tissue specialization, the branched structure and modular development. All higher plants are constructed from repetitions of the same basic modular structure, leaf plus bud and below-ground root meristems, repeated many times, but the numbers can vary enormously. Since a plant can be regenerated from a single meristem, redundancy in tissue development is self-evident. Furthermore, growth regulators often overlap in their effects. This is organizational plasticity we simply do not understand. But plants can be best viewed as more like a democratic confederation in their control structure rather than an autocracy as occurs in animals, controlled by an all-embracing nervous system. With a spatial and temporal mosaic of resources that surround the plant, some latitude must be present to allow the local but growing tissues to optimally exploit rich sources. Our understanding of plant intelligence must therefore accommodate these properties and answer some very basic questions: how many varieties of behaviour can be constructed with a limited number of tissues; does partial independence in the behaviour of individual growing tissues change a holistic view of plant intelligence?
Individuality is used to describe situations in which morphologically or anatomically identical cells, tissues or plants show non-similar responses to signals (Trewavas, 1998; Gilroy and Trewavas, 2001). The example of rhizome gravitropism quoted above (Bennet-Clark and Ball, 1951) details individual variations. Individuality receives little or no investigation in plant science despite being a widespread phenomenon. As if to counteract the paucity of different tissues in the normal vegetative plant, continued embryogenic development by meristems results in tissues and cells with enormous varieties of individual behaviour. A reservoir of different cell behaviours becomes available to enable construction of a variety of tissue and plant behaviours to exploit the resource mosaic. Individuality of the kind commonly observed in plants might be unique. A mechanism for individuality has been proposed as originating from stochastic variation in the distribution between daughter cells of tiny numbers of critical proteins controlling cell and tissue development (Gilroy and Trewavas, 2001; Federoff and Fontana, 2002).
Recognition of individuality can easily be seen from dose-response curves. If the responses are all-or-none [e.g. germination (the seed does or does not germinate), root formation, abscission, flowering, dormancy, senescence, etc.], then a dose-response curve simply reflects population variation in sensitivity to the inducing stimulus (Trewavas, 1991; Bradford and Trewavas, 1994). Such dose-response data can vary over three to five orders of magnitude change in the strength of the inducing stimulus, thus indicating the degree of individual variation (Trewavas, 1981). Nissen (1985, 1988a, b) compiled much information on this point using growth regulators as the controlling stimulus.
Individuality in guard cells
Because the behaviour of individual guard cells can be easily examined, I have used them as an illustration. Figure 1, published in Raschke (1988), quantifies the response of stomatal apertures in Commelina to increasing abscisic acid (ABA) concentration. The concentration range spans six orders of magnitude, but even then some guard cells have still not closed completely. Yet, at each concentration, an increasing number of stomata close, suggesting that the individual dose-response range can be much narrower than that of the whole population. The population response is thus made up of differential sensitivity amongst individual guard cells to ABA. Furthermore, by quantifying chlorophyll a fluorescence (Raschke 1988), temporal variation in the rate at which individual guard cells closed in the intact leaf was detected. After ABA treatment, patchiness in closure rates was observed. Further information is summarized by Mott and Buckley (1998, 2000).
Fig. 1. Frequency distribution of stomatal apertures in illuminated strips from the lower epidermis of leaves of Commelina communis, floating on 80 mM KCl, plus the indicated concentrations of (±)-ABA. f, Fraction of stomata in a particular aperture class; w, stomatal aperture. The upper scale represents aperture-class numbers and shaded columns represent the fraction of closed stomata. Reproduced with permission from Raschke (1988)
Many signals have been described as regulating guard cell closure (
Willmer and Fricker, 1996). If there is equivalent individual cell variation for each of these signals, as described for ABA, then enormous potential exists to construct many kinds of leaf water relation behaviours under a variety of environmental conditions. Each novel behaviour is constructed by putting together unique collectives of guard cells in both space and time. Such behaviour can be regarded as adaptively variable and thus coinciding with the definition of intelligence in foraging for carbon dioxide.
Mott and Buckley (2000) indicate that guard cell collectives (recognized as patches during closure) can behave coherently, chaotically and may oscillate in total aperture and vary in size and character as predicted from above. Crucially, patch behaviour is underpinned by definite evidence of communication across whole areas of leaf and between individual guard and epidermal cells. Such communication may result from hydraulic interactions, but much further investigation is needed to distinguish other anticipated mechanisms, such as electrical and chemical communication. Detection of oscillations in transpiration rate may result from this dynamic (Johnsson, 1976).
In the whole leaf, the most sensitive guard cells could potentiate the response of other local but less sensitive guard cells to closing signals by modifications of: (1) internal humidity; (2) abscisic acid sequestration; (3) carbon dioxide; (4) wall pH; (5) wall potassium and calcium levels; and (6) the osmotic behaviour of subsidiary and other guard cells (Willmer and Fricker, 1996; Mott and Buckley, 2000)—all factors known to modify aperture. The most sensitive cells might then act as critical elements in the propagation of information relating to aperture throughout local regions of the leaf; acting perhaps like relays in an excitable tissue. Sensitive guard cells could then be regarded as analogous to motor cells (organizing centres as described by Winfree, 1987), generating focal points that organize stomatal patch formation by influencing the behaviour of other guard cells. The rate of patch formation and its longevity would then be dependent on the local density of the most sensitive (motor) guard cells. Is intelligent behaviour to be sought in the network composed of the most sensitive cells?
Support for this possibility comes from the observations of Rascher et al. (2001). They showed that variations in crassulacean acid metabolism (CAM) in leaves are the result of localized but initially independent oscillators that eventually cooperate to produce the whole leaf circadian CAM response, in a fashion analogous to guard cell communication. Oscillators are characteristic of motor cell initiation and control (Winfree, 1987), and oscillations in activity are common in neural networks.
Other examples of individuality
Other cellular examples of individuality have been reported in gibberellin-dependent amylase production by aleurone protoplasts and in pericycle cells sensitive to auxin (Gilroy and Trewavas, 2001). Further observations of individuality have been made in cotyledon cells, in anthocyanin synthesis responsive to red light, and cytoskeletal structure responsive to blue light (Nick et al., 1992, 1993). Tissue examples can found in fruit ripening and abscission (Trewavas, 1998).
If individual guard cell behaviour is a paradigm for other cells in other tissues, then the following can be suggested. Individuality in aleurone cell amylase production enables potential optimization of amylase production within the variety of environmental states experienced by cereal seedlings. A computational network can form slowly or quickly, but sugars, amino acids and fatty acids will be some of the information transmitted between individual aleurone cells (Trewavas, 1988). Pericycle cells more sensitive to auxin or other factors will act as foci for the formation of branch roots. The different sensitivities of individual pericycle cells act to provide a broad range of lateral root production in different root environments. Using a microbeam of red light, Nick et al. (1993) observed great heterogeneity in the formation of red light-induced anthocyanins between individual cotyledon cells, as described earlier. They reported patchy formation of the pigment and indicated that there was substantial variation in the sensitivity of individual cells. Furthermore, not all cells that likewise synthesized chalcone synthase mRNA in response to red light also synthesized anthocyanin, and long-range suppression of one group of cells by another was observed. Communication is clearly happening, but the mechanism of communication has not been established. But again, anthocyanin formation can be optimized to fit the environmental requirements and to improve overall fitness.
The benefits of individuality are to be found in the much greater variety of response provided to the individual plant. Williams (1956) provided an interesting way of assessing the variation in populations (Box 1).
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