Download The Evolution of Plant Action Potentials

J. theor. Biol. (1983) 103, 645-648
LETTER TO
THE
EDITOR
The Evolution of Plant Action Potentials
Electrical signals which resemble nerve impulses are widespread in plants
at all levels of evolution from the Algae to the Angiosperms, and have
been well reviewed (Pickard, 1973; Sibaoka, 1966,1969). They are caused
by the depolarization
of cellular membrane potentials and like nerve
impulses, propagate along the cell membrane. Sometimes they can be
transmitted from cell to cell for long distances via the plasmodesmata. In
several higher plants they have a proven function in communication,
for
example, they transmit information about the arrival of prey in the insectivorous plants of the Droseraceae, they trigger the movement of floral
parts to assist insect pollination in several other plants, and they control
the seismonastic movements of Mimosa pudica. However, action potentials
which have no obvious nervous function can also be found, for example,
periodic depolarizations of unicells such as Acetabufaria have been observed (Norvac & Bentrup, 1972). Also in higher plants there is often considerable spontaneous electrical activity resembling action potentials which can
be detected by electrodes placed on the plant surface. These signals are
thought to be due to the depolarization of individual cells within the plant
body detected electrotronically
at the plant surface. They do not seem to
show true propagation far (if at all) beyond their cell or origin (Pickard,
1973). It seems likely, therefore, that these signals have no function in
long-distance communication.
If action potentials which have no function in communication
are widespread, even in the lower organisms, it is reasonable to suppose that they
arose for some other purpose and that their role in communication
has
been secondarily acquired. What then is their primary function? A possible
answer to this question comes from the study of cell membranes and their
associated membrane
potentials.
Membrane
potentials are virtually
ubiquitous in both the animal and plant kingdoms, with the insides of cells
being typically about 100 mV negative to the outside. These potentials are
maintained by the activity of various electrogenic ion pumps (Higinbotham,
1973) and, amongst other things, they provide the energy for the active
transport of many substances across the membrane (see Baker, 1978 for
a review). If membrane potentials perform such important vital functions,
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GOLDSWORTHY
why do cells not involved in nervous conduction periodically depolarize
themselves by exhibiting action potentials?
A possible answer is that the first action potentials evolved as a response
to injury to enable the cell membrane to be repaired. It would seem very
likely that membranes which have been damaged must be depolarized
before they can be repaired. A typical potential of 100 mV produces a
voltage gradient of 10’ volts per metre across a 10 nm thick membrane.
Were such a gradient to occur in air it would cause a lightning discharge!
When it occurs across a hole in the membrane, it would be expected to
cause such a rapid flux of ions through the breach that repair could well
be impossible. The action potential may have arisen in evolution as a
mechanism for rapidly switching off the cells membrane potential while
the damaged membrane was being repaired, the signal for it to occur being
the partial depolarization brought about by ions leaking through the injured
region. It is well established that plant action potentials can be induced by
both injury and artificial depolarization.
As in animals, the plant action potential is caused by the opening of
voltage-sensitive ion channels in the membrane in response to a localized
depolarization.
This depolarizes the membrane further, and causes even
more ion channels to open in neighbouring regions of the membrane so
that a wave of depolarization spreads over the cell surface. The ion channels
are programmed to close after an interval so that the original membrane
potential can be restored. I would suggest that the period of depolarization
is that necessary to conduct an average repair. If the repair is not completed
in this time and the cell remains partially depolarized in the damaged
region, a further action potential is innitiated after a short refractory period,
and the whole process may be repeated many times. In practice a whole
series of action potentials can be seen to propagate from the site of a
massive injury to a plant (see Pickard, 1973).
This hypothesis explains why spontaneous action potentials are widespread in plant tissues where they do not appear to propagate beyond the
cell of origin and have no known nervous function. It also explain why
these signals tend to originate in growing regions of the cell (Norvac &
Bentrup, 1972), where movements of the expanding cell wall are likely to
cause localized tearing of the plasmalemma. The observation that turgor
changes after watering plants which have wilted induce action potentials
is also consistant with this hypothesis, since this too is likely to produce
relative movement between the cell wall and the plasmalemma.
If we accept this hypothesis for the evolutionary origin of action potentials, it is relatively easy to see how they could have evolved further as a
means of communication.
Although their primary function may have been
LETTER
TO
THE
EDITOR
647
to depolarize the membrane prior to repair, action potentials propagating
rapidly from a site of injury would also serve as a useful signal that injury
had occurred, and their number and frequency would indicate the severity
of the injury. It would not be surprising if natural selection then occurred
to produce appropriate injury responses which were controlled by the
receipt of such action potentials. The cessation of protoplasmic streaming
which accompanies an action potential down an internodal cell of Nitella
(Sibaoka, 1966) is perhaps an example of this in plants.
With the arrival of complex multicellular
plants, it became possible,
although not mandatory, to transmit action potentials from cell to cell via
the plasmodesmata. These appear to have many of the characteristics of
electrotonic synapses, transmitting the signal only under certain circumstances (Sibaoka, 1966). This would then permit a rapid response by a large
area of the plant to a localised injury. Although most of the “spontaneous”
action potentials in plants do not propagate far, if at all, beyond their cell
of origin, action potentials following massive injury, such as the burning
of a leaf can be detected propagating for long distances through the phloem
of many plants. One might argue that this is due to injury to the conducting
cells and the very open nature of cellular communication at the sieve plates
to give a conducting pathway analogous to a nerve axon. However, in
most cases, there is no obvious response in higher plants to the receipt of
an action potential, although changes at the biochemical level cannot yet
be ruled out. Although propagating action potentials and the infrastructure
to support them are widespread in plants, it is only in those plants which
respond by showing rapid movements that we have definite proof of their
function in communication.
Plants which show rapid movements in response to action potentials
have arisen independently at many diverse points in evolution, raging from
the insectivorous plants of the Droseraceae, through Mimosa in the
Leguminosae to the motile stamens of the barberry. These plants initiate
their action potentials in response to touch rather than injury, but the
mechanism could still be very similar. All that is needed is for certain cells
of the plant to be hypersensitive so that permeability to ions is increased
by relatively minor mechanical deformation. Such cells occur just below
the tentacle head in Drosera and at the base of the trigger hairs in Dionaea.
They respond to mechanical stress as if they had been injured. They first
become depolarized, generating the so-called receptor potential which triggers action potentials which propagate through the neighbouring cells to
the motor regions. Little is known of the trouch transducing process, and
it is not yet possible to say whether the receptor potential and its consequent
action potentials are as a result of a genuine membrane injury or to some
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A.
GOLDSWORTHY
more sophisticated mechanism. However, whatever the present mechanism,
it is reasonable to suppose that it may have evolved from something simple,
like a hypersensitivity to injury.
We may therefore conclude that while most plants have little need of a
nervous system as sophisticated as that of higher animals, at least some of
them have a system comparable with that of the lower forms of animal
life. The use of action potentials may be a case of parallel evolution from
a membrane repair mechanism in a common ancestor.
Department of Pure and Applied
Imperial College,
London SW7 2BB
Biology,
(Received 22 September 1982)
REFERENCES
BAKER, D. A. (1978). New Phyrol. 81,485.
HIGINBOTHAM.
M. (1973). A. Rev. Plant. Phvsiol. 24.25.
NORVAC,
B. & BENTRUP;
F. W. (1972). Plaita
108,i27.
PICKARD,
B. G. (1973). Bot. Rev. 39, 172.
SIBAOKA,
T. (1966). Symp. Sot. exp. Biol. 20,49.
SIBAOKA,
T. (1969). A. Rev. Plant Physiol. 20, 165.
A.
GOLDSWORTHY