Aspects of plant intelligence (ii)
Darwin's views on selection had emphasized equally the importance of the environmental conditions of life alongside competitive selection. 53
“In my opinion the greatest error which I have committed has not been allowing sufficient weight to the direct action of the environment”. 104 In Darwin 105 under the heading of “Direct and definite action of the external conditions of life” Darwin summarizes some of the evidence that concerns his “error” referred to above. I suspect that a goodly number of Darwin's observations (1868) are due to transgenerational inheritance that is common in plants. 53 Darwin's appreciation of environmental influences are indicated in Darwin 105 and the following chapters.
The supposed randomness of genome mutation was not based on actual evidence but supposition stemming from X-radiation damage to the genome in the 1920s. Recent research has shown that mutations in the genomes of bacteria, fungi, animal and plant are not randomly distributed. Cells use DNA repair and target repair to certain critical genes and those frequently transcribed. 106-109 The cell overrides mutation randomness; it's not left to chance. 56 , 110-112 The book by 110 describes where the current understanding of life is incomplete or often wrong.
Increasing knowledge of genome structures and sequences, starting with Barbara McClintock's studies, has generated the concept of natural genetic engineering: cells manipulating their overall genome structure. 113 , 114
The basic unit in evolutionary change is the cell which is alive; not the gene. 110
A molecule of DNA contains enormous numbers of base sequences coding for genes. Their meaning is only apparent inside the cell.
Genes are often regarded as central to plant biology but only because they can be modified and act as memory. The richness and meaning in protein–protein interactions and their structures is far greater than speculation on the role of genes. 115
Jablonka and Raz 116 describe the critical relevance of transgenerational inheritance via epigenetic modification of the genome as indicating Lamarckian, not Darwinian, inheritance. 116 Transgenerational inheritance can last anywhere from 1 to 9 generations. 53 , 117
A supposed barrier to separate reproductive from somatic cells. No such barrier exists in plants. The cells that construct the vegetative meristem are usually the parents of those that construct the reproductive meristem. Other modern synthesis failings are described in Noble. 112
The necessity to incorporate teleonomy (teleology) into evolutionary explanations.
“Giving organisms purposes and goals is a profoundly adaptive strategy, for it equips them to act as agents” Ball. 110 Teleonomy evolved because it increased reproductive fitness. 118 , 119
Corning 98 has proposed a theory of evolution incorporating purpose. However, the evidence provided for this theory derives predominantly from animal examples. Purposive goal-directed interactions within individual plants and between plant species and non-species members are so endemic that any new construction of a theory of evolution has to include purposive behavior of plants as a strong contributory element to individual species survival.
The kind of evidence that could be included for a general theory of goal-directed processes could be convergent evolution in plants. Fifteen examples are published in Trewavas 12 and more are to be found in Gilroy and Trewavas. 53 Transgenerational inheritance; that is, the purposeful provision to siblings of parental experience who live within local parental environments. Diecious species; male flowers only in N-poor environments. The genotype via pollen moves from the local poor area. Female flowers are synthesized in N-rich environments, areas that are good for seed growth and subsequent siblings. 12 p. 184. The ubiquity of leaf-like structures in all phylae. 53 Cambial appearance and development, the goal being to increase trunk size, to demarcate resources to advantageously placed shoots 12 p. 105 and to outgrow competitors. Reaction wood supports larger branches. In damaged stems, cambial interruption regenerates the ring structure 12 p. 110. Bisecting apical meristems leads to regeneration of two new meristems. Numerous adaptive behaviors improving the probability of survival. As for evolutionary direction, plant form and function are constrained by physical laws that could provide some semblance of overall evolutionary direction. 53 Those that don't obey the physical principles don't survive. These suggestions are some obvious examples. Each represents purposive behavior. The hypothesis needs a plant review in its own right.
According to Pfeffer, 120 there at least a dozen tropic phenomena. If any or all of these are adaptive, then fail-safe mechanisms of some kind should exist to deal with anomalous environmental variation and the potential problems of cellular noise. Out of these, responses to gravity and light corner most research.
I have chosen gravitropism because sufficient evidence indicates that there are two gravi-sensory systems in plants. Textbooks often provide a simple diagram of gravitropism using statoliths. In my many years of teaching, such simple models, and the adherence to them, create the view amongst biological students that plants are indeed simple organisms; nothing of interest worth further study 120 (p. 211) states that sensitive roots and seedling stems perform slight curvatures in response to a centrifugal force equivalent to 0.001 g. The sensitivity indicated by this measurement, in itself, raises issues about mechanisms, particularly whether statoliths could sense such tiny stimuli.
The current mechanism of gravitropic responses identifies starch statoliths as the sensing component and currently it is well-established. But is starch always available? Thalmann and Santelia 121 have reviewed the conditions under which starch is depleted and it is, unsurprisingly, stressful conditions. These are conditions likely to be frequently experienced in wilderness. And even if some starch is unavailable, Kiss 122 has argued that full statolith size is necessary for full gravitropic sensitivity. Inadequate starch content is then likely to interfere with the anticipated alignment to the gravity vector, impacting on the probability of survival and diminishing adaptive behavior. Is the present model of gravitropic behavior lacking an essential fail-safe alternative?
Using aequorin-transformed Arabidopsis seedlings and rotating them on a wheel initiates a rapid calcium transient lasting less than a minute but followed by a much slower calcium transient peaking after several minutes and followed by a decline lasting some 30 minutes or more (Plieth and Trewavas). 123 Many publications report that placing a vertically growing tissue on its side initiates rapid electrical changes often within 30 seconds to one minute). 124-134 These electrical changes can last for 25–30 minutes or longer 124-126 and occur both in the shoot tip and the zone of expansion.
When laid flat, the lower side becomes more positively charged than the upper, thus altering the internal electrical field structure. 126 Becoming more positively charged can be considered to result from the increased entry of wall calcium into the cells. Reducing the establishment of an electrical gradient between the two sides of a tissue gradient by shunting the external electrical potential reduces gravitropic bending by a half. 131 Gravi-stimulation of intact Arabidopsis roots also initiates a calcium wave moving from the tip to the growing region similar to auxin movement 135 but again just on the lower side. Initiation and propagation of variation potentials may be a possible further consequence. 136
Lipid rafts can move around the plasma membrane, dictated by the shape and structure of the cellular electrical field. 137 PIN 2 must be a moveable protein to accommodate auxin movement for different spatial directions during tropic bending. 138 It can be suggested that PIN2 is simply located in a lipid raft. As the relevant ionic field changes, it will move around the plasma membrane to the appropriate position to divert the auxin stream and alter growth, as indicated in the standard auxin-based theory of gravitropism.
Firn and Digby 139 (p. 135) reference eight papers that show removal of the tissue tip (the statocyte region), left stumps that were still gravi-sensitive. These authors also reported that the outer epidermal layers constrain normal growth. Caspar and Pickard 140 ; Pickard and Thimann 141 reported that “starchless” plants still express a strong gravitropic behavior in seeds, roots, flower stalks and hypocotyls. Edelman 142 stripped the vascular tissue and associated statocytes from cereal coleoptiles and in separate plants, removed the root tip. Both manipulated tissues still exhibited a strong gravitropic response. Single-cell plants respond meaningfully to gravitational change and direction 143 ; Roux et al. 144 ; Salmi et al. 145 .
If a vertically growing epicotyl or hypocotyl is laid flat on a surface, the cells on the lower side experience compression from the weight of the tissue above; those on the upper side experience tension. If instead the tissue is held at one end, a frequent observation is that the tissue bends as a result of its weight. 124 , 125 Again, greater compression on the lower surface, tension on the upper. Compression and tension are mechanical signals. The act of laying a vertically growing tissue in a horizontal position constructs a mechanical gradient between the lower and upper side. Individual cells will experience this gradient with the maximal difference between the epidermal layers on the top and bottom.
Mechanical signals are interpreted via mechano-controlled calcium channels. 146 The expectation is a gradient of [Ca2+]I signaling from the lower to the upper side. Developing and growing plant cells in these tissues experience these mechanical forces through the viscoelastic structure of the cytoplasm. The energy available from this simple mechanical signal is estimated at 1 dyne/cm. Root and shoot cells respond in opposite ways to tension and compression.
An analogous stimulus is a single touch on one side of a vertically growing tissue. When this is performed, the side which is touched experiences compression and the untouched side tension. Bose 124 (p. 437) illustrates a simple device for permanently touching a stem and showed that touch induces a curvature kinetically similar to that of gravity. Single transient touch signals also initiate a [Ca2+]i transient, lasting about 20 seconds, 147 or calcium waves. 87
The nucleus is the largest and heaviest organelle of eucaryotic cells. During cell development the nucleus is specifically positioned, suspended, and held in place by actin-based cables attached to the plasma membrane and microtubules that are sensitive to control by [Ca2+]i. 148-151 Mechanical forces on cells are transmitted into the cell via the conductive and viscoelastic cytoskeleton and impact directly on the nucleus itself. 149 , 151-153
Just as there is a gradient in compression/tension within a single tissue, there will also be a gradient in Ca2+ entry between the upper and lower plasma membranes of the cells in these tissues. When a cell is experiencing compression, [Ca2+]I entry likely disaggregates some local actin cables, probably through the Ca2+sensitive gelsolin. This will permit slight downward movement of the nucleus or even slight deformation of nuclear structure. 148 , 152 , 154 The extent of nuclear movement in different cells of a tissue laid flat will reflect its position in the compression/tension gradient. The cytoskeleton will experience the compression change too. Entry of Ca2+ into the cell via the plasma membrane is known to cause the local accumulation of the highly negatively charged PIP2 on the inner plasma membrane. 155 Aggregated PIP2 in turn attracts proteins that act as actin nucleation sites, 156-159 enabling new actin cables to regrow and encompass the nucleus. This is called an actin refit.
Via Lamins in the nuclear envelope, these new cables penetrate the nuclear envelope and then attach to the nuclear actin, whose known function is chromatin remodeling. 160 Recovery and resetting of these new actin cables resets the nuclear position. Contraction of these new actin cables acts via nuclear actin to expose new chromatin regions for transcription. Specific wall loosening enzymes (e.g. plasma membrane H+ ATPase) are synthesized. The compression gradient will therefore be mirrored by a wall extension gradient causing the tissue to bend.
This hypothesis offers a route for investigation and testing its validity being based in part on what is established and now needs further examination.
The above mechanism, using changes in [Ca2+]I and nuclear repositioning, indicates how plants without statoliths can still function gravitropically. It may also be the mechanism that enables single plant cells to respond to gravitational signals. Salmi et al. 145 observed a discrete change in calcium current as the single cell responded to a gravity change. This mechano-transductive, actin refit, alternative can now help explain results that previously lacked explanation.
Learning and memory are the bases of all forms of intelligent behavior: artificial intelligence; immune intelligence; swarm intelligence; human intelligence and biological intelligence. A memory cannot be acquired unless it is first learnt. Memory is a direct indication that learning has taken place. This requirement for learning rules out the kinds of behavior which in animals were formerly regarded as instinct. When environmental conditions interrupt or threaten the completion of that life cycle, adaptive behaviors are invoked, enabling the identification of plant behavior as intelligent. 2
Barron et al. 161 have collected 58 different definitions of learning and presented a composite definition. “A common umbrella concept that can be applied across disciplines by considering learning simply as the processing of information derived from experience to update system properties”…… “That will facilitate the integration of evolutionary approaches to learning.”