The overall process of gravity sensing and response processes in plants may be divided conveniently into at least four components or stages: Stimulus susception (a physical event, characteristically the input to the G receptor system of environmental information about the G force magnitude, its vector direction, or both); information perception (an influence of susception on some biological structure or process that can be described as the transformation of environmental information into a biologicallly meaningful change); information transport (the export, if required, of an influence (often chemical) to cells and organs other than those at the sensor location); and biological response (almost always (in plants) a growth change of some kind). Some analysts of the process identify, between information perception and information transport, an additional stage, transduction, which would emphasize the importance of a transformation from one form of information to another, for example from mechanical statolith displacement to an electric, chemical, or other alteration that was its indirect result. These four (or five) stages are temporally sequential. Even if all that occurs at each stage can not be confidently identified, it seems evident that during transduction and transport, matters dealt with are found relatively late in the information flow rather than at the perception stage. As more and more is learned about the roles played by plant hormones which condition the G responses, the mechanism(s) of perception which should be are not necessarily better understood. However, if by asking the right questions and being lucky with experiments perhaps the discovery of how some process (such as sedimentation of protoplasmic organelles) dictates what happens down stream in the information flow sequence may be made

Brown, Allan H.

English

NASA Technical Reports Server

N90-13948
GRAVITY RECEPTORS AND RESPONSES
Allan H. Brown
Gravitational Plant Physiology Laboratory
University City Science Center
3401 Market St., Suite 350
Philadelphia, PA 19104-3323
OVERVIEW---Comp0nents of G sensing and response processes in plants.
The overall process may be divided conveniently into at least four components
or stages: (a) Stimulus susception: a physical event, characteristically the
input to the G receptor system of environmental information about the G force
magnitude, its vector direction, or both; (b) Information perception: an
influence of susception on some biological structure or process that can be
described as the transformation of environmental information into a
biologically meaningful change; (c) Information tri_nsport: the export, if
required, of an influence (often chemical) to cells and organs other than
those at the sensor location; and (d) biological response: almost always (in
plants) a growth change of some kind. Some analysts of the process identify,
between (b) and (c), an additional stage, iransduction, which would emphasize
the importance of a transformation from one form of information to another,
for example from mechanical statolith displacement to an electric, chemical,
or other alteration that was its indirect result.
These four (or five) stages are temporally sequential. Even if we cannot
confidently identify all that occurs at each stage, it seems evident that during
transduction and transport we must be dealing with matters to be found
relatively late in the information flow rather than at the perception stage. As
we learn more and more about the roles played by plant hormones which
condition the G responses, we are not necessarily able to understand better the
mechanism(s) of perception which should be our focus in this Session.
However, if by asking the right questions and being lucky with our
experiments perhaps we can discover how some process (such as
sedimentation of protoplasmic organelles) dictates what happens down stream
in the information flow sequence.
GRAVITY FORCE AS A CONTINUOUS VARIABLE
Gravity is different things to different specialists. To some, nominal zero G
is a stress to which hominids "adapt." Chronic G forces above zero but less
than unity may seem important as experimental conditions chiefly to discover
if there is a G threshold above which certain stress responses (euphemistically
called adaptation) can be endured without progressive unacceptable sequelae.
From that view point unit G is especially important as a "control," easily
accessible on earth and supplied in orbit only by a centrifuge. However, plant
and animal physiologists who work with small organisms are apt to consider
gravity not necessarily as a stress but in a general sense as an _nvirgnm_n_ial
factor--one of the top three or four in order of importance to organisms.
Like other conditions that affect plants these scientists must be able to control
experimentally the G force vector direction and intensity over the full range
of possible G levels from nominally zero to as far above 1 G as may seem
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scientifically interesting. Thus, viewing G as a continuous experimental
variable, we tend to think of the control condition not as 1 G but as
weightlessness. Unit G becomes one of many abscissal G levels that occur
when plotting the G function of a particular biological effect. This view point
has not been readily accepted by some experts in space medicine; it is
widespread in the general biological community.
GRAVITY SENSING AS A CENTRAL QUESTION FOR UNDERSTANDING
HOW GRAVITY IS IMPORTANT TO PLANTS
For the better part of a century, plant physiologists have recorded a large
number of descriptive studies of plant responses to gravity --more precisely
to experimentally controlled changes in the direction in which the earth's
gravity force acts on the plant. Relatively recent advances in methodology
and improved biological and biochemical background information have
encouraged the belief that we may be on the verge of dramatically improved
understanding of the mechanism(s) by which gravity is sensed and those by
which biological responses are generated. Nevertheless, we are still at a stage
in our science where purely descriptive studies are urgently needed. Only
infrequently have our theories been challenged by decisive experimental
tests. Since the experimental potential for gravitational physiology has been
dramatically enhanced in the last three decades by the promise of full control
over the total range of experimentally applied G forces, a large number of new
questions arise which call for new exploratory experiments to describe
quantitatively the gravity sensing process in test organisms. Gravity sensing,
although not a new area of study, has enjoyed greatly increased priority as a
process to be studied by new methods created or enhanced by space flight
technology. Physiologists, each in his own phylogenetic area of choice, seem
to be in at least intuitive agreement that scientific progress is highly likely in
the area of gravity sensing by exploiting the new technology. Broadly stated
the question is: How is gravity important to plants? The central question that
now drives most experimental designs is: How does the organism sense
gravity?
TOOLS FOR EXPERIMENTATION
Exploration or experimentation with biological responses to any
environmental factor requires control and quantitative manipulation of the
factor of interest, in our case, the gravity force. It is interesting that the
three major tools needed for creating, maintaining, or simulating G levels are
all rotating machines.
The centrifuge probably is the most familiar. In earth laboratories
centrifuges have been used to impose G forces ranging up to about 500 G for
long periods in exploratory experiments with small plant seedlings (Gray and
Edwards, 1955; Brown, 1983). For small organisms only a few G units above
normal may be considered non-stressful and can contribute to studies of G
sensing in the hypergravity G range (Brown et al, 1975). At much higher
forces (10s or 100s of G units) stress reactions patently dominate even though
the test species often adapts morphologically to growth in the strange
environment.
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For application to space experimentationvarious advisory groups have
repeatedessentially the same recommendationurging a "1 G control" aboard
the spacecrafts although only recently has the recommendationbeen
implemented,first by Soviet and later by ESA experimenters.
A unit G control in spacealso would be subjectedto all known and unknown
artifactious influences of the spacecraft (shock and vibration, for example)
and of its environment (especially ionizing radiation). If all such artifacts
were understoodand could be measured,it would be possible to perform
adequatecontrol experimentson earth. However, skeptics always will be hard
to convince that there are not some unknown influences which could deceive
the investigators. The least expensiveway to allay such fears would be to
provide the often recommended1 G control centrifuge in space even though
the important issue really has little to do with biological effects of G forces g.cd
se. There remains, as a most compelling argument for flying on-board
centrifuges, the need to access the hypogravity region of the G parameter,
0<G<I. (Cf. contribution of D. K. Chapman in this report.)
Potentially the unit G condition also can be achieved in space by rotating
the space vehicle about its center of mass. However, if we want not merely to
avoid the necessity for humans' adaptation to microgravity but also want to
carry out scientific experiments in hypogravity, a centrifuge would still be
required, in that case with its rotational axis exactly coincident with that of
the rotating space vehicle.
The centrifuge has been used on earth to extrapolate data from a series of
tests at different hypergravity G levels to the ordinate axis intercept which
thereby becomes a qualified estimate of what value of the measured parameter
would obtain if the test could be performed at zero G. The qualification of
course, is the assumption of linearity (or some other function) beyond the
range accessible to experimentation. In a very few cases the assumption of
linearity was disproven but at this stage of our understanding of the effects of
protracted hypogravity it is impossible to generalize.
The clinostat (Sachs, 1882) is another rotating device widely used by plant
physiologists to simulate hypogravity conditions on earth. It is described and
evaluated by D. K. Chapman in this report. The simulated condition of zero G,
achieved by clinostatting generally is referred to as "gravity compensation".
How well that condition gives biological responses which are the same as those
of tests in free fall remains a question that must be addressed empirically. Less
than a handful of such comparisons have been accomplished and the
conclusions were not in agreement (Lyon, 1968; Merkys et al, 1975; Brown et
al, 1974; Brown and Chapman, 1984). It does not seem prudent to generalize at
this stage of our science (Brown et al, 1976).
The rotating machine most recently added to our list of tools for
experimentation is the spacecraft in earth orbit, Its radius of rotation (about 7
x 106 km) is somewhat larger than that of our earthbound centrifuges and
clinostats. Its rotation rate in near earth orbit is much less (approximately 2 x
104 Hz). In stable circular orbit the G force at the center of gravity of the
spacecraft closely approximates zero in the sense that no force other than
gravity perturbs it; thus it establishes the ideal condition of free fall.
135
By itself, the spacecraft in orbit is theoretically capable of providing only
one G value, nominally zero. However, by combining the satellite's potential
with the capability of an onboard centrifuge, an experimenter can attain a
protracted G force environment of any desired intensity, from zero to however
much his experiment requires. The centrifuge is neededto impose a
controlled, constant, centripetal force on the test subject otherwise in a state
of free fall.
It may be of interest, for those experimentswhich require a very low G
environmental condition, that the centrifuge axis should remain parallel to
the orbital axis of rotation of the spacecraft. Whether the spacecraftis gravity
gradient stabilized, or rotates slowly in its orbital plane, makes little
difference: However, rapid spacecraftmaneuverscan produce gyroscopic
effects which shouldbe considered. They may or may not be small enough to
be ignored.
TO SENSE GRAVITY DOES ANYTHING HAVE TO MOVE?
Gravity perception can be accomplished by a variety of different
mechanisms. Given that something is being influenced by gravity (or by an
equivalent inertial force) that influence can be detected by dozens of physical
or physical chemical mechanisms devised by engineers and physicists as welt
as by those, whose numbers we are in doubt, that were invented by biological
systems in the course of their evolution.
For those devices invented by scientists, their mechanisms seem to have
nothing in common except that all are based on ways of detecting movement.
Many such devices have been invented and their detectors, amplifiers, and
methods of readout are diverse. It would be arrogant for us to pretend that
biological means for detecting mass movement are so much less sophisticated
that only one or even only a few methods of gravity detection are employed by
organisms. Nevertheless, over the past century plant physiologists have been
prone to generalize (at least implicitly) the amyloplast sedimentation
mechanism not only as the earliest process in G perception but as if it were, in
principle, the only device plants learned to use for detecting gravity
susception.
To put the matter in perspective three things should be kept in mind. (a)
In spite of widespread occurrence of patently sedimenting organelles
(statoliths such as large starch-filled amyloplasts or inorganic crystals, viz.
barium sulfate) there are numerous examples of gravisensitive plant organs
whose cells do not contain mobile organelles sufficiently more or less dense
than the cytosol so that they sediment under conditions that prevail for G
responding plants. According, in statocytes devoid of starch loaded
amyloplasts some less obvious mechanism must exist to account for the evident
consequences of gravity susception. Where no obviously functional statoliths
have yet been found, we should not assume that those cells are incapable of
sensing gravity. (b) It is impossible for any bioaccelerometer or for any man-
made device to detect the susception of gravity unless something moves.
Whether we call the perturbation falling, twisting, stretching, bending,
compression, displacement, stratification, sedimentation, acceleration, or
altered momentum cannot change the fact that the act of susception must be to
alter something's position, shape, or acceleration. That categorical conclusion
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is basedon a fundamental physical principle. (c) Gravity is a body force.
Acting on every particle of mass in an object, it imparts to that object its
weight. An inertial force also is a body force. Acting on every particle of
mass in an object, if unopposed, it gives to that object an acceleration.
According to the Principle of Equivalence, it is quite impossible for
experiments to differentiate between inertial forces and gravitational forces
within one frame of reference. By placing an object in earth orbit it becomes
weightless because it continues to be acted on only by a gravitational force.
Therefore it is better to refer to its condition as free fall rather than as zero
gravity. All other forces that could oppose free fall and establish equilibrium
(hence weight) are absent. A particle of mass in orbit is at rest in an inertial
reference frame. It remains in uniform motion as long as no other force acts
on it. Because inertial and gravitation forces are equivalent, a centripetal
force of any desired magnitude applied to theparticle produces the same effect
as would a gravitational force of the same magnitude. This is the basis for
establishing a 1 G "control" condition in a satellite.
A suggested subtopic of this Session Item was, "Could gravity responses be
pressure responses?" In the sense that a pressure change is suggested as an
alternative to a movement, the answer is emphatically no, for reasons stated
above. However, whatever moves could be responsible for (or a consequence
of) a pressure change. Pumping up a flat automobile tire, for example, leads to
both a small amplitude movement (centimeters) and large change of pressure
(from ca. 100 k Pa to ca. 300 k Pa). It is of no consequence that we are
accustomed to measuring tire inflation with a pressure gage instead of a tape
measure (unless we "eyeball it" in which case the distention is estimated, not
the pressure.)
With respect to plant cells, BjOrkman (1988) argued against a G sensor
mechanism based on cells' manometric versatility, among other reasons
because of the large normal fluctuations of resting pressures in plant cells.
Normally cells in growing organs carry a mean pressure of about 300 to 600 k
Pa above atmospheric (101.3 k Pa). However, over time during the growth
process and under different conditions of water availability, extremes of
internal pressures in plant cells may fall as low as -1500 k Pa and as high as
+2000 k Pa, limits which are conservative estimates. Such enormous
fluctuations would make it very difficult for a plant organ to detect (and to
reliably interpret as gravity induced) pressure changes of very much smaller
magnitude.
Moreover, by bending and restraining gravisensitive plant shoots and
roots, the contralateral stretching and compression of the growing organ does
not "fool" the G sensing mechanism. When released from constraint the
tropistic response proceeds as would be expected from an apically located
sensor that perceives only the G vector. Thus it becomes, if not impossible, at
least very awkward to attempt construction of a G sensing theory that depends
at any stage on a bioaccelerometer measurement of internal cell or tissue
pressure.
CONCLUSION
In both animals and plants those responses which follow the act of sensing
gravity ultimately involve whole organs---often the whole organism. Cell
specialization is well developed in higher organisms that sense gravity. In
137
plants the sensor function usually residesmostly in a small group of cells, less
than 1% of total tissuemass(rarely in only a single cell). Thesecells, the
sensingorgan, is sometimesreferred to as a bioaccelerometer. It respondsto
gravity susceptionalways by somekind of movement. In most casesthis
involves sedimentationof mobile organellesor stratification of zones of the
cytoplasm. There is no evidence that G perception involves cooperation
between cells although the consequencesof G sensing undoubtedly show
summationof activities of all sensorcells. Thus G perceptionin plants is a
uniquely cellular function as it must be where it is accomplishedin
unicellular forms. The sensing-responseprocess can be divided, at least
conceptually, into several stages. Recent advanceshave told us more about
how organisms, especially plants, use the gravitational information they
acquire. When we are able to fully exploit the potential of experiments in
microgravity and at any other gravity level the experiments require, we may
find progress on how plants acquir_ gravitational information may
outdistance that on other areas of gravitational biology.
REFERENCES
Bjtirkman, T. 1988. Perception of gravity by plants. Adv. Botan. Res. 15: 1-41.
Brown, A.H. et al. 1974. A comparison of leaf epinasty induced by
weightlessness or by clinostat rotation. Bioscience 24: 578-520.
Brown, A.H. et.al. 1975. Morphology of Arabidopsis grown under chronic
centrifugation and on the clinostat. Plant Physiol. 57: 358-364.
Brown, A.H. et al. 1976. Limiation on the use of the horizontal clinostat as a
gravity compensator. Plant Physiol. 58: 127-130.
Brown, A.H. 1983. Resistance of mature Arabidopsis plants to mechanica
deformation in relation to G-force during development. The Physiologist
26 (No.6) Suppl. 149-150.
Brown, A.H. and D.K. Chapman. 1984. Circumnutation observed without a
significant gravitational force in spaceflight. Science 225: 230-232.
Gray, S.W. and B.F. Edwards. 1955. Effects of centrifugal forces on growth and
form of coleoptile of wheat. J. Cell. Comp. Physiol. 46:97-126.
Lyon, C.J. 1968. Wheat seedling growth in the absence of gravitational force.
Plant Physiol. 43: 1002-1007.
Merkys, A.J. et al. 1975. The development of seedling shoots under space flight
conditions. Life Sciences and Space Research 13: 53-57.
Sachs, J. 1882. Uber Ausschliessung der geotropischen und heliotropischen
Krummungen wahrend des Wachsens. Arb. Bot. Inst. zu Wurzburg 2: 209-
225.
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Gravity receptors and responses

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