Intelligence requires a network of elements capable of adaptively variable information flow to underpin intelligent behaviour. In animals, nerve cells are specifically adapted by structure to enable rapid phenotypic adjustments and computation. But, critically, a network requires communication between the elements.
Communication in neural systems
Much early work in the last century hinged on the notion that communication across nerve synapses and throughout the brain was purely electrical. Action potentials jumped across the synaptic divide propagating further action potentials downstream. A contrasting view suggested that communication between nerve cells was performed solely by chemicals, although these in turn would generate action potentials down the long axon. Neurotransmitters were released by fusion of secretory vesicles with the plasma membrane. Specific neurotransmitter receptors across the synapse induced a new action potential by modifying ligand-operated ion channel function. The chemical messenger theory is correct: 99 % of all communication in the brain is chemical (Greengard, 2001). Action potentials are used primarily to speed communication down the long nerve cell axons.
Two kinds of chemical transmission are recognized. Fast transmission, completed in milliseconds, uses the neurotransmitter glutamate and glutamate receptors; fast inhibition uses -aminobutyric acid (GABA). Slow transmission can take many minutes and is enormously more complex, involving at least 100 different chemicals falling into four classes: biogenic amines, peptides, amino acids and nitric oxide (Greengard, 2001). Quite remarkably, glutamate has recently been found to influence cytosolic [Ca2+]i in plant cells and nitric oxide is a recognized second messenger in plant cells (Dennison and Spalding, 2000).
Communication between and within plant tissues
That the various parts of plants communicate with each other has been established by many experiments. Various surgical treatments (such as removal of root or shoot or leaves, mimicking predation or other damage), resource stress (lack of light or water or minerals) or exposure of one part of a plant to varying resource levels, give rise to specific changes in growth and development elsewhere in the plant, indicating communication of the stimulus. Such phenomena have been called correlations. In these above cases, development is usually adjusted to try and recover a balance between root and shoot or to ensure a better balance of basic resources. [Note, again, the presence of a goal (set point) and an error-correcting (learning) mechanism.] Flowering, tuberization, bud break, enhanced root growth and branching can follow selective exposure of leaves to particular light periods. Signals are thus transmitted from the leaf to other tissues (Trewavas, 1986b).
Shortage of specific resources leads to accelerated growth of the tissue (either as elongation, weight or branching) that normally collects the resource. In contrast, abundance of all resources leads to increased branching or, if the resource is localized, often local branching. When shaded, shade-intolerant species show substantial elongation of the primary stem (at the expense of lateral stem growth), increased leaf area and a disproportionate reduction in the growth of fine roots (Bloom et al., 1985). Shortage of water leads to enhanced root growth and particular proliferation when an abundance of resources is located. Lake et al. (2001) observed that high CO2 levels reduce stomatal frequencies, but the CO2 signals are sensed by mature leaves and the information conveyed to developing leaves which cannot respond to high CO2. Communication of aphid attack between plants has recently been shown to involve other volatiles (Petterson et al., 1999).
By use of a microbeam of red light, Nick et al. (1993) provided convincing evidence for cell-to-cell communication between cotyledon cells with long-range inhibition of gene expression in un-irradiated cotyledon cells at some distance from the irradiated patch. Moreover, the cell regions responding were, in turn, specifically determined by the region irradiated, suggesting selective communication only between certain cells in the cotyledon.
The information that is being communicated between tissues and cells is now known to be extraordinarily complex. Communication involves nucleic acids, oligonucleotides, proteins and peptides, minerals, oxidative signals, gases, hydraulic and other mechanical signals, electrical signals, lipids, wall fragments (oligosaccharides), growth regulators, some amino acids, secondary products of many kinds, minerals and simple sugars (Bose, 1924; Gilroy and Trewavas 1990, 2001; Jorgensen et al., 1998; Sheen et al., 1999; Mott and Buckley, 2000; Sessions et al., 2000; Kim et al., 2001; Nakajima et al., 2001; Brownlee, 2002; Haywood et al., 2002; Takayama and Sakagami, 2002; Voinnet, 2002; references on growth regulators in Quatrano et al., 2002). Transcripts can even move between graft unions (Kim et al., 2001). From the current rate of progress, it looks as though plant communication is likely to be as complex as that within a brain. The demonstration of macromolecule movement between cells is of considerable significance because it enables substantial amounts of information to be built into the signal if needed; thus complex information can be encoded in the signal.
Plasmodesmata controlling information flow
Plasmodesmatal connections enable movement of proteins and nucleic acids as well as smaller molecules between plant cells (Zambryski and Crawford, 2000). Movement of transcription factors and nucleic acids has the potential to activate or repress genes in cells remote from the source by activation of DNA methylation or by mRNA translation; oligonucleotides with specific sequences can silence genes. To create a complex, cellular network capable of computation also requires particular cellular locales for specific receptors remote from the source of the signal. Alternatively, substantive variation in sensitivity to the same signal between individual cells might achieve the same end.
Furthermore, just as synaptic connections (dendrites) can be increased to amplify particular pathways of communication during learning, individual cells can modulate the extent of plasmodesmatal transport. Physiological alterations of plasmodesmatal transport result from anaerobic and osmotic stress, or changes in [Ca2+]i or inositol phosphates (Ding et al., 1999). I expect this list to increase. Even slight changes in growing conditions have been observed to modify signal transmission (Zambryski and Crawford, 2000). Quantitative and qualitative changes in plasmodesmatal number occur during development, and secondary plasmodesmata can be formed in the absence of cell division and can even branch rather like the synthesis of new dendrites.
Plasmodesmatal connections seem to be limited to adjacent cells. Whether plasmodesmatal strength, analogous to synaptic strength, could be increased is not clear but, intriguingly, one of the proteins that binds plasmodesmatal proteins is pectin methylesterase (Jackson, 2000). Such observations might imply that connections between plasmodesmata and the wall can be altered and that mechanical constraints alter plasmodesmatal function leading to a modified flux of information. In this case wall interactions could control the ability of plasmodesmata to act like an information valve, changing flux rates according to mechanical stresses imposed either by the environment or resulting from mechanical stresses induced by growth.
Communication within cells
Communication within cells is equally complex, and stable and transient transduction complexes are known to be used to interpret new information (Gilroy and Trewavas, 2001). Cytosolic Ca2+, [Ca2+]i, in particular, seems to act as a cellular second messenger with ubiquitous roles in signal transduction and intracellular communication. [Ca2+]i has very limited cytoplasmic mobility, and enhanced entry through channels following signalling activates Ca2+-binding proteins within the microdomain in which channels are clustered (Trewavas, 2002a). Localized intracellular distributions and particular control properties of channels and ATPases that pump Ca2+ back into subcellular compartments or walls result in Ca2+ waves and oscillations (Mahlo et al., 1998; Schroeder et al., 2001), a rich source of information and specific communication. Rapidly moving Ca2+ waves have been observed in a number of cell types and thus can act to coordinate parts of the recipient cell towards a behavioural objective (Sanders et al., 2002). The wave moves on the surface of cellular membranes, most probably the endoplasmic reticulum (ER) and inner plasma membrane surface. The wave itself is a movement of Ca2+-induced Ca2+ release and not a physical transmission of Ca2+ ions. Topological similarities between Ca2+ waves and simple neural circuits enabling aspects of computation to be understood have already been drawn (Trewavas, 1999).
Many different environmental signals (e.g. touch, wind, cold, disease, gravity, etc.) modify [Ca2+]i and are responsible for generating phenotypic plasticity. How can a single ion mediate such response variety? The reality is that [Ca2+]i is just one of a large number of signals that operate in signal transduction, but one that acts as a nodal point in a robust transduction network. Complexity in [Ca2+]i signalling is increased by contributions from various organelles, such as the nucleus, ER or chloroplast (Van der Luit et al., 1999). The nucleus is thought to have its own Ca2+ mobilizing system, and mitochondria and chloroplasts have internal Ca2+ control. The ER and the vacuole modify cytoplasmic signals (Sanders et al., 2002). Different closing signals in guard cells elicit Ca2+ responses from different compartments (Gilroy and Trewavas, 2001). The amplitude and kinetics of the Ca2+ transient (wave) and different regions of the transient can also initiate discrete transduction sequences. Changes in [Ca2+]i can be extremely rapid (within the 100 ms range) and can initiate selective changes in gene expression. Changes in [Ca2+]i are also essential to communication and learning within nerve cells (Greengard, 2001).