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INTRODUCTION |
Biological rhythms are usually
classified according to their period length or frequency. Those
rhythms exhibiting periods less than 20 h are termed
ultradian. A major difficulty encountered in contemplating
the possible mechanisms giving rise to ultradian rhythms is
that they exhibit a spectrum of frequencies. Even in one
experimental system (Mimosa pudica), one encounters a range of period lengths ranging from seconds to minutes to hours (Roblin, 1977
). Although these movements are all ultradian, it is unlikely that
they are manifestations of the same fundamental rhythm.
Unlike circadian rhythms, ultradian rhythms, for reasons both practical
and philosophical, have received little attention from plant
biologists. Chief among the practical causes is the fact that ultradian
rhythms are readily overlooked in experiments in which observations are
made only intermittently (Due, 1989). Typically, the vagaries of data
that occur during discontinuous measurements
are either ignored or attributed to sampling error or
poor technique rather than to biological rhythmicity. Secondly, the common practice of pooling and averaging data collected from different specimens will serve, given that no two specimens are likely to be completely in phase, to obfuscate rhythmicity.
It is important to recognize how philosophically ill-equipped
modern plant physiology is to accommodate the study of ultradian rhythms. Ultradian rhythms are best studied in single specimens, using
high-resolution, non-perturbing continuous recording techniques. Such a holistic approach to physiology runs counter to the
prevalent reductionism that emphasizes the pooling and averaging
of data collected from destructive measurements, usually upon as many specimens as practicable.
This month's column concerns an especially enigmatic subclass of
spontaneous ultradian periodicities, here referred to as 0.1- to 10-Hz oscillations.
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0.1- to 10-Hz Oscillations: A Physiologist's Nightmare |
Most botanical researchers have ignored 0.1- to 10-Hz rhythms for
two reasons. First, because the amplitudes of these rhythms are so
small, it is easy to dismiss any single report as artifactual. The
number of researchers, however, who have convinced themselves that 0.1- to 10-Hz rhythms are real is not small (this review is by no means
exhaustive), and the possibility that all have been hoodwinked by
subtle artifacts seems unlikely. A second reason why 0.1- to 10-Hz
rhythms have engendered so little interest among plant
physiologists is that they are fickle: They appear and disappear spontaneously. This fickleness has no doubt frustrated many
researchers. Several reports are but breathless descriptions of some
"newly discovered" 0.1- to 10-Hz phenomenon and of
promises
ultimately unfulfilledof more exciting data
to come. Yet another reason for the neglect of 0.1- to 10-Hz
rhythms is that even when they do occur, they often exhibit short-term
variations in amplitude and frequency. Their fickleness and variability
make them virtually impossible to explore pharmacologically. Indeed,
such basic questions as whether 0.1- to 10-Hz oscillations are
endogenous or exogenous, or affected by anoxia, metabolic inhibitors,
or low temperature, remain unanswered.
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The Discovery of 0.1- to 10-Hz Oscillations |
Kashyap (1932), in an essentially anecdotal report, was the first
to discover a 0.1- to 10-Hz rhythm in plants. During a botanical field
trip to Sikkim on a still day in July 1930, he observed closely the
leaves of Molineria capitulata (formerly Curculigo recurvata). He wrote that "... a leaf would begin to perform
to and fro movements all of a sudden, go on for about a half-minute or
so and then stop by itself. All of the other leaves of the plant would
be absolutely still and no leaves of any other plants in the
neighbourhood would show any movements... Sometimes it so happened
that when one leaf had finished the movement another leaf of the same
plant would take it up a little later... The rate of movement
varied a good deal, between 40 to 120 complete
oscillations per minute." Kashyap reported that some cultivated
specimens in Gangtok also showed the movements, although more
feebly and only in the morning. He was unable to observe the
movements in specimens that he grew in Lahore. Nevertheless, he was
able to capture the phenomenon on a cinematographic film, which he
later presented at the Indian Science Congress.
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0.1- to 10-Hz Leaf Movements Are Coupled to Bioelectric
Rhythms |
Semenenko (1972) used platinum plate electrodes and an
electroencephalograph equipped with a frequency analyzer to record spontaneous electrical oscillations in several species of higher plants, including Mimosa pudica, Phaseolus
vulgaris, Primula veris, and Begonia
lucerna. These oscillations exhibited frequencies of 0.2 to 0.5 Hz
and amplitudes of 100 to 250 µV. The frequency and amplitudes of the
oscillations depended on the time of day, the pulsations being most
pronounced at dawn and at dusk. Moreover, Semenenko (1972) asserts
that frame-by-frame time lapse photography reveals that the plants
exhibit rhythmic movements that resemble the electrical rhythms in
form. Contemporaneously with Semenenko (1972), three additional
research reports were published concerning the spontaneous occurrence
of low-amplitude, 0.1- to 10-Hz bioelectric rhythms in plants
(Karlsson, 1972; Pickard, 1972; Reinhold et al., 1972).
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0.1- to 10-Hz Oscillations Are Unlikely to Be Related to
Action Potentials (APs) |
The most popular hypothesis to account for 0.1- to 10-Hz
bioelectric oscillations in higher plants attributes them to trains of
APs elicited by a single cell or a small cluster of cells within the
vicinity of the electrode (Pickard, 1972; Glebiçki et al., 1986).
A major problem with this hypothesis is that it does not take into
account the relatively long refractory periods (typically on the order
of 10 min) that immediately follow plant APs. Although repetitive
trains of APs can be elicited in higher plants (e.g. Ping and Lou,
1990), their frequencies are, under physiological conditions, generally
about two orders of magnitude lower than the 0.1- to 10-Hz
oscillations. A second problem is that 0.1- to 10-Hz oscillations,
unlike typical plant APs, do not propagate (Pickard, 1972).
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Are 0.1- to 10-Hz Oscillations Related to Geomagnetic
Pulsations? |
Fraser-Smith (1978) found that the spontaneously arising
geomagnetic variations of smallest amplitude (0.05-0.1 nT) and
shortest period (0.2-5 Hz), the Pc1 class of geomagnetic pulsations,
could be readily detected in an oak tree using two nails as electrodes. In fact, the resolution of the tree was not too much worse than that of
a nearby loop antenna (a 20,000-turn steel-cored solenoid). Such
geomagnetic pulsations gave rise to approximately 100 µV amplitude
electric potential oscillations in the tree. The virtually identical
occurrence and spectral characteristics of the geomagnetic pulsations
measured by the tree electrodes and by the conventional geophysical
recording equipment indicated that the tree potentials were largely
induced by time variations of the geomagnetic field. To investigate
this possibility further, Fraser-Smith circumnavigated the tree with a
portable search coil powered by a 1-Hz signal generator. He found that
a 1-Hz oscillation of the potential difference between the tree
electrodes was produced only when the search coil was oriented with its
moment vector in the north-south direction. When the two electrodes
were moved to the north face of the tree, a response could be observed
only when the search coil was oriented in the east-west direction.
Pc1 pulsations change during the 11-year solar cycle (Saito, 1969).
During descending years in the solar, such as 1930 and 1971-1972, Pc1
pulsations are rare on geomagnetically quiet and moderately disturbed
days. However, during the main phase of the magnetic storms that occur
during these years, Pc1 pulsations of a special kind, the so-called
"pearls with diminishing periods" are noted (Saito, 1969). At mid
and low latitudes, the diurnal variations of Pc1 pulsations show maxima
during the early morning hours and the evening (Saito, 1969). A typical
characteristic of Pc1 pulsations is a tendency for them to recur on
consecutive days, approximately at the same hours, or to disappear for
days and even weeks. Semenenko's electroencephalograph recordings of plants are virtually identical to pearls with diminishing periods in
terms of their amplitudes, periods, fickleness, pearl necklace-like appearance, and favored time of occurrence. In light of Fraser-Smith's (1978) findings, it appears that plants do act as antennae for these
weak geomagnetic variations. The mechanism and the reasons why they do
remain mysterious, but this property of plants may go a long way in
explaining the anomalous 0.1- to 10-Hz rhythms recorded in
plants
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INTRODUCTION
0.1- to 10-Hz Oscillations:...
