In nervous systems, new connections (dendrites) between nerve cells may form the basis of memory (Kandel, 2001) and loss of the dendrite coincides with loss of memory. What is required for memory is an ability to access past experience so that new responses incorporate relevant information from the past. Many different forms of plant memory can be envisaged, all of which modify signal transduction, from the current chemistry and enzymology of membranes (Gilroy and Trewavas, 2001) or wall characteristics (Trewavas, 1999), to prior expression of particular genes. It is also clear that the history of stimulation modifies subsequent transduction (Ingolis and Murray, 2002) and, in plants, intepretation through [Ca2+]i is likewise modified by previous signalling, ensuring another form of memory is present (Trewavas, 1999). All these forms of memory can be recognized by the ability to interact with, and modify, the transduction pathways to new signals. The only requirement is merely that the memory can be accessed and can influence the response to the current signal. A more complex form of memory requires information storage of previous signalling, with the ability to retrieve the information at a much later time. Both forms occur in plants.
Memory of developmental status.
It is obvious that the present state of development acts as memory for any individual plant because the same signal can have different effects determined by when the plant, tissue or cell receives it. The effects of blue or red light signals are good examples, having different effects dependent on the stage of development. Thus, red light can affect leaf movement, stem elongation or germination. Furthermore, photoperiodic plants can be exposed to one or two inductive photoperiods and then returned to a non-inductive light/dark schedule where they will continue to flower. Some long-lived memory has obviously been instituted. Plants that are vernalized by 3 weeks’ low temperature, or appropriate imbibed dormant seeds given 3–4 weeks’ low temperature, retain the memory of that treatment and either flower or germinate when the inductive schedule is no longer imposed. Lloyd (1980) suggested that flowering consists of a series of reassessment points in which adjustments to the final number of flowers could be made dependent on nutritional availability, in a form of learning and memory. If seed imbibition takes place in conditions that are inimical to germination then a more prolonged state of dormancy—secondary dormancy—can be entered into, lasting many years (Trewavas, 1986a). Some dormant imbibed seeds can show annual flushes in germination rates, often in the form of damped oscillations in numbers, germinating over successive years. Many aspects of dormancy are analogous to nervous memory; there are short- and long-term versions, dormancy can be reinforced or overridden, and a variety of environmental facets interplay to modify germination and dormancy. Even the molecular basis of long-term dormancy may be similar to animal memory (Trewavas, 1986a). Apolar Fucus zygotes can be polarized by a 1-s flash of intense directional blue light, and so on. Examples abound.
In the whole plant there are many examples where prior signals modify the response to rapid subsequent signals, thus indicating memory of the previous signal. Dostal (1967) describes many such examples produced by himself. For example, exposure of de-etiolated flax seedlings to white or red light generally has no influence on cotyledonary bud growth. But if the main stem above the cotyledons of flax seedlings is removed, both cotyledonary buds grow out. When Dostal removed one cotyledon and the main stem from flax seedlings and placed the truncated seedling in white light, only the axillary bud subtended by the remaining cotyledon grew. But when placed in red light the opposite bud grew out. Both buds retrieve information concerning the presence or absence of the apex and will have received signals to grow. But retrieval of that information can be subsequently overridden for either bud by other later signals arising from light exposure, the wavelength of light and the presence or absence of the cotyledon.
In Scrophularia nodosa, information retrieval by dormant buds is evidently modified by the state of development (Dostal, 1967). This plant has square-shaped stems, dichotomous branching and, thus, known vascular arrangements. Cuttings were made from pieces of stem containing two opposite leaves and thus two axillary buds. If kept moist, both axillary buds break dormancy and grow; adventitious roots form on all four sides of the base of the cut stem. However, if the leaves were mature, removal of one of the leaves inhibited growth of the subtended axillary bud whilst permitting the other bud to grow out. Adventitious roots then formed only on the side of the amputated leaf. If the leaf left behind was not fully mature, inhibition of axillary bud growth was still evident, but the roots developed on the opposite side underneath the remaining leaf. If the leaf left behind was developmentally very young, both the axillary bud and roots grew out only on the leaf side. There is thus a complex interplay between age of leaves, leaf removal, bud outgrowth and root formation that modifies the original excision signal, but the memory of that signal remains in the activity of the buds.
Retrieval of information after a delay
Similar experimental approaches in Bidens pilosa have shown that the initial signal can be separated from its effects by many days. Removal of the growing apex from young seedlings again results in outgrowth of cotyledonary buds (Desbiez et al., 1991). Puncturing one cotyledon of non-decapitated plants had no effect on the cotyledonary buds which remained quiescent. But if one cotyledon was pricked with a needle, both cotyledons then removed within 5 min, and the seedling then decapitated several days later, the bud opposite to the pricked cotyledon started to grow much faster than the other. An asymmetrical state had been achieved, but usually in only about half of the seedlings. The response is clearly an example of individuality. The recall of information about the original needle damage required the seedling to be in the appropriate state. Various environmental treatments, such as cold or warm temperatures, could override the retrieval of information that specified asymmetry. It was thought that a wave of depolarization was the signal conveyed to the bud from the puncture signal on the cotyledon. The overriding environmental treatments are all known to modify [Ca2+]i.
Ca2+ controls the accessible memory of environmental signals involved in the induction of flax epidermal meristems (Verdus et al., 1997). These hypocotyl meristems could be induced by drought or wind signals, which are also known to increase [Ca2+]i transiently. But induction required a depletion of seedling Ca2+ for about 1 d before the effects of drought and wind could be detected. Using this system, memory of the previous drought and wind signals could be stored and accessed for at least 8 d unabated, before expression was finally elicited by a Ca2+ depletion. The mechanism is unknown, but changes in gene expression or protein kinase activity resulting from drought and wind signals might be responsible.
Further examples of shorter term memory involving [Ca2+]i have emerged. Exposure of etiolated cereal leaves to red light results in unrolling. However, sections of leaf will not unroll in red light if Ca2+ is removed from the medium (Viner et al., 1988). But if leaf sections are exposed first to red light, Ca2+ can be added back to the medium to induce unrolling up to 4 h later. Some excited state of the cells is induced by red light and is maintained for at least 4 h. Administration of a hyperosmotic shock normally induces a [Ca2+]i transient of short duration (Takahashi et al., 1997). But if the shock is administered in the absence of extracellular Ca2+, the transient fails to appear until extracellular Ca2+ is returned to the medium. The separation of shock and return of extracellular Ca2+ can last as long as 20 min.
Accessing of internal information; is the niche an accessible memory?
It is perhaps no accident that maximal fitness is the overall goal of any individual animal, and intelligent behaviour contributes to that goal (Wright, 1932; Dawkins, 1976). Wright (1932) used the metaphor of an adaptive landscape to produce a visual representation of fitness in which individuals represent hills or mountains with the maximally fit being the highest.
The operational life cycle goal to which all individual plants aspire is also maximal or optimal fitness. However, fitness is indissolubly linked with the local environment in which the individual finds itself and grows. Maximal fitness can be achieved when the plant grows in its optimal (fundamental) ecological niche. The niche is difficult to characterize (Bazzaz, 1996, and see below) and, with competition for resources in wild plants, is limited to the realized niche. But measurements show that the niche is individual to the genotype, not the species. On that basis it is likely that each individual plant will possess a unique niche memory to which it will attempt to match growth and development. The important feature is that information, which describes the fundamental niche, is present in the organism and can be accessed, thus representing a kind of long-term (life cycle) memory. How information about the fundamental niche can be inherited, when it is rarely realized (Hunt and Lloyd, 1987), is not understood.
Theoretical and experimental work suggests that species must have different resource requirements for them to co-exist in a community; they must occupy different niches with only a minimum of overlap. Furthermore, recognition must be present, i.e. information encoded in the individual, that indicates when the niche conditions are met and when they are not. Since all plants require minerals, water and light, niche differentiation is considered more difficult to define in plants than in animals, where the concept first arose (Bazzaz, 1996). However, if the concept is useful it should inform upon the subject matter of this essay.
Phenotypic (and physiological) plasticity represents part or all of the error-correcting mechanisms that individual plants use in an attempt to achieve optimal fitness in the realized niche. Phenotypically plastic mechanisms are not reflex responses (see below) but depend on an ability to assess not only what tissues should alter (with the assessment influencing very early tissue development), but an ability to stop plasticity when sufficient change towards the optimal goal has been made. However, to have to resort to phenotypic plasticity implies that optimal fitness may not be achieved. Individual plants that express plasticity will more nearly approach the fitness objective than individuals that do not. But the error-correcting mechanism must involve complex negative feedback mechanisms with versions of trial and error; that is, learning.
Inherently, all descriptions of niche must basically concern the interaction of the plant with its environment, that is the position of the individual in both space and time (Wright, 1932). Moreover, the niche can differ for plants grown in the laboratory compared with those in the wild. Uniform stands of some plants such as wild wheat, Phragmites and Spartina are known to exist and may even be genetically identical. But most plants exist in complex communities implying discrimination by the individual plants amongst the numerous factors in the environment. It is known that wild populations contain enormous genetic diversity (Burdon, 1980) and it is thought that this reflects, in large part, environmental diversity which must be correspondingly complex (Antonovics, 1971).
Many plants do show different (non-equitable) physiological and morphological responses along gradients of any of the primary resources, and it seems unlikely that many or, indeed, any of these resource axes act independently of each other (Tilman, 1982; Bazzaz, 1996). Some resources, like N or K, can act synergistically but others can be incongruent; an increase in sunlight can institute moisture stress for example. If there are about 15 environmental factors acting in differing degrees and affecting the perception of each other then the combination of possible environments in which any individual can find itself and to which it must respond is enormous. Thus, the necessity for learning rather than rote behaviour. Moreover, long- and short-term responses to environmental variables will be different.
The response of an individual along a resource gradient is very strongly influenced by its neighbours. While negative interactions through competition for the basic resources of space, light, minerals and water, and interactions through allelopathy, are well established (e.g. Turkington and Harper, 1979; Turkington, 1983; Zangerl and Bazzaz, 1984), cooperative, positive interactions are clearly evident through mycorrhizal spread, symbiotic relations with bacteria, releasing nitrogen to other plants, remediation of local stressful environments (Salzman and Parker, 1985) or semio-chemicals warning other plants of predatory attack (Petterson et al., 1999).
Time may be an additional critical factor in defining niche. Continued growth generates new environments for both root and shoot, and responses of both tissues to the environment change ontogenetically. In low vegetation, above-ground patchiness may be imposed by the spatial arrangement of dwarf shrubs and persistent clumps of perennial herbs and modified by microtopography and grazing. Hartgerink and Bazzaz (1984) observed that the imprint of a footprint on the soil, or a stone placed nearby, could accelerate germination rates but substantially reduced final biomass and seed number nearly three-fold, reducing fitness. Such results suggest a remarkably fine definition of the environment by the individual plant. Soil resources can be patchily distributed or may be continuous (Farley and Fitter, 1999).
Individual genotypes of Polygonum expressed unique norms of reaction in physiological, allocational and morpho logical characters (including fitness) when nutrient and light environments were modified [Zangerl and Bazzaz, 1984; Bazzaz, 1996 (note response surface on p. 168); Sultan, 1996, 2000; Sultan et al., 1998]. Thus, at each setting of the environment, the individual plant can access information that it can use to construct a response and to ensure that overall, maximal fitness will be achieved. The implication is that the difference between the optimal niche/phenotype and the present environment and present phenotype can be measured. A counterbalancing response is then constructed that directs the individual into a new trajectory of development. Once again a goal is specified even though that goal might be heritable and an error-correcting mechanism is in place to try and achieve the goal. Constant monitoring of the new phenotype as it develops and continuous control are exerted to ensure that the new phase of development is optimal and consistent with long-term evolutionary objectives. Information about the individual genotype can be accessed as permanent memory and interpretation follows from interaction with the complex network that underpins signal transduction processes. Until we understand better the properties of signal transduction networks, we will not be in a position to understand how plants achieve their fitness goals.