Tải bản đầy đủ - 0trang
IV. Forces Exerted by Roots and Shoots
MECHANICAL RESISTANCE OF SOIL
Others again enable the meristem to evade stress, as does the nutant habit
of the seedling shoot in many dicotyledons.
It is not proposed to go into further detail here, as clear accounts of
mechanical adaptation are to be found in the literature. The most comprehensive source of information is still Haberlandt’s classical text
“Physiologische Pflanzenanatomie.” Numerous further examples of the
mechanical adaptations to be found in underground shoots are given by
Leonhardt ( 1915).
In Pfeffer’s experiments part of a root or shoot was secured within a
gypsum block; a second but movable block was then cast around the
exposed tip or around one side of the organ, Any force exerted on the
second block by the growing organ could then be measured by balancing
against a known resistance. In practice Pfeffer was concerned solely
with static equilibria, measuring the resistance that had to be applied to
the second block to prevent it from being moved.
Pfeffer found that when an organ was so confined it soon exerted a
force. The force increased rapidly at first and then more slowly, approaching a maximum in 2 to 3 days. The maximum force corresponded to a
pressure of from 5 to 10 bar distributed over the largest cross section
within the growing region. Although he did not make many measurements, Pfeffer’s results suggest that the pressure exerted by root tips is
greater in the direction of the longitudinal axis than in the radial direction (see Table 11).On the other hand, Pfeffer found that the axial and
Pfeffer’s Data on the Maximum Pressure Developed by Confined Root Tips0
Axial pressure (bar)
Vicia faba L.
Zea mays L.
T: 17-20°C; length of tip
Transverse pressure (bar)
< 1 cm.; pressure
radial pressures developed by shoots were similar. Pfeffer was not altogether surprised by the magnitude of the pressures that he recorded
for roots and shoots, as Muller (1872) had found previously that a
mechanical pressure of 14 bar was needed to prevent the elongation of
pith isolated from the stem of the sunflower, Helianthus annuus L., and
K. P. BARLEY AND E. L. GREACEN
Krabbe (1884) had reported that a radial pressure of 10 bar was needed
to prevent an increase in the girth of trees.
After the publication of Pfeffer’s paper in 1893 the subject appears
to have been neglected until Williams (1956) measured the force exerted
by the arching hypocotyl of small-seeded legumes. Although papers of
Gill and Miller (19%) and Barley (1962) helped renew interest in the
topic, these authors were mainly concerned with the efEects of stress on
growth (see Section V, A, 3 ) . Recently, Barley and Stolzy ( 1966) have
described a method of measuring the force exerted by root tips penetrating a soil. The soil is supported by a force transducer that measures the
reaction to the root tip. Providing measurements are restricted to the
time during which the hairless part of the tip is penetrating the soil, only
a small correction is needed for skin friction.
From Pfeffer’s work it is clear that, for a given species and organ, the
pressure developed is largely independent of the diameter attained, so
that the force exerted increases with the size of the growing organ. Even
though roots apply a smaller pressure in the radial than in the axial
direction, the force exerted in the radial direction is by far the greater, as
the pressure acts over a larger area. For example, roots of the broad bean,
Viciu faba L., can exert maximum radial and axial pressures of 5 and 9
bar, respectively, but the radial and axial forces that can be exerted by
a 4 cm. length of root are 5 kg.wt. and 0.3 kg.wt. The upward acting
forces exerted by seedling shoots range from 15 g.wt. for the thin hypocotyls of alfalfa, Medicago satiua, L., (Williams, 1956) to 401) g.wt. for
the thick hypocotyls of the broad bean (Pfeffer, 18913). Evidently, any
environmental factor that changes the dimensions of a growing organ
influences the total force that can be exerted on the surroundings.
The ability of roots or shoots to exert force on the soil depends not
only on their physiological properties and shape, but also on the anchorage provided by the proximal parts of the plant; that is, the force exerted
cannot exceed the ability of the proximal parts to withstand the reaction.
Anchorage is provided by skin friction together with the resistance that
has to be overcome to dislodge the seed, root hairs and root laterals.
Pfeffer found that forces of the order of 40 g.wt. per centimeter length
were required to pull the hair-covered radicles of broad bean from soils,
and that several centimeters of branched root could stand a pull equal
to the maximum axial force exerted by the growing tip of the root.
1. Osmotically Induced Turgor
The exertion of force by plant organs is most readily explained in
terms of their osmotic behavior. When pressures are measured with
MECHANICAL RESISTANCE OF SOIL
respect to the ambient solution as datum, for a semipermeable tissue at
where x = osmotic pressure of the cell contents, and T = hydrostatic
pressure within the cell. Strictly, an equilibrium expression for an imperfectly permeable osmometer should be given here, but the nature of cell
permeability does not affect the present argument. We disregard variaand T within the turgid cell, arising from the presence of
differentially permeable cytoplasmic membranes. Treating forces directed
toward the center of the cell as positive, at the cell wall,
where W = pressure exerted by the wall (“wall” pressure); B = pressure
exerted by other cells (“tissue” pressure); and P = pressure applied
externally by the plant.
Thermodynamically, osmotic and swelling pressures are identical
(Hermans, 1949); so, if we assume that meristematic cells offer little
internal resistance to water transfer, then the vacuolar liquid and protoplasm should be in or near osmotic equilibrium. Further, providing
supply of water is not limiting, osmotic equilibrium with the ambient
solution is thought to be attained, or nearly so, throughout the zone of
cell enlargement ( Ordin et al., 19.56).
If plant forces are osmotic in origin, they may be mobilized either
by an increase in x or by relieving W and B . The pressure exerted by
W = B = 0.
the plant attains a theoretical maximum, P,,,,, = x ~ when
Pfeffer believed that both processes were operative. Measuring ro with
the plasmolytic method of de Vries (1884) and with the “minimum
length” method often ascribed to Ursprung (1923) in modern texts,
Pfeffer (1893) concluded that in broad bean T o rose gradually after the
root tip or seedling shoot had been confined, Secondly, Pfeffer showed
that elastic strain disappeared from the cells of confined root tips. He
found that root tips confined for 48 hours or more failed to shrink when
plasmolyzed. This was not due merely to maturation of the apical
tissue, as the tips at once began to elongate when transferred to iced
Unfortunately, as Pfeffer used potassium nitrate as the osmoticum,
his r0 values are excessively high ( > 15 bar). It is now known that this
salt penetrates excessively into root cells. Using sucrose at 2”C., Barley
(1962) did not find any increase in x in compressed growing radicles of
the tick bean (Viciu faba L., var. MINOR). Neither Pfeffer nor Barley
detected any increase in T in compressed radicles of corn. Whether or
not there is a buildup in x in some species, the relief of wall and tissue
K. P. BARLEY AND E. L. GREACEN
pressure appears to offer a ready means of mobilizing osmotic turgor to
perform external work. Although the plant material is not directly comparable, it is interesting to note that the value of P,,, found by Pfeffer for
the root tips of corn agrees with the r,,value obtained by Barley: P,.,,
= To = 11 bar.
2. Nonosmotic Contributions to Turgor
Even if we can account for the magnitude of the pressure measured
by Pfeffer without the need to invoke other than osmotic processes, this
in itself does not show that osmosis is the only process involved. However, no other process has conclusively been shown to raise the hydrostatic pressure within plant cells. Bennet-Clark ( 1959), having reviewed
the evidence in favor of “active” uptake of water by plant cells, suggested
that the strongest evidence was provided by data showing the osmotic
pressure of expressed sap to be generally less than the plasmolytically
determined value. A more straightforward explanation of this discrepancy, however, is provided by the tendency for osmoregulation to
occur during exposure to an osmoticum, either by solute transfer or by
hydrolysis of cell polymers.
In commenting on the water relations of Nitella, Dainty (1963) notes
that although small differences in electrical potential across charged
pores might theoretically lead to substantial turgor differences across
the membranes concerned, such differences could not in fact be realized
in Nitella as outward flow can occur through numerous uncharged pores.
Similar reasons may rule out electroosmotic or other “active” contributions to turgor in higher plants, but at present too little is known about
the properties of cell membranes for us to decide.
3. Other Forces of Metabolic Origin
So far we have considered only those forces that depend on cell
turgor. We also need to ask whether forces might not arise from the
propensity of growing tissues to accumulate, synthesize, or transform
materials other than water. A sol + gel transformation, for example, is
associated with cell division; before furrowing begins protoplasmic sols
are converted to gels. Furrowing and cleavage are then brought about
by the contraction of the gels, and energy used in building up the
structure of the gel can be expended as work as the gel contracts and
reverts to a sol (Landau et al., 1955). Forces that might be associated
with the surface extension of the cell wall or cell membranes also need
to be considered, whether or not they are adsorptive in origin as Bell
Although such phenomena provide interesting examples of ways in
MECHANICAL RESISTANCE OF SOIL
which metabolic energy may be expended as work, it has to be remembered that the rigidity of meristematic tissue is almost wholly dependent
on cell turgor. When the tissue is turgid, the cell walls cannot themselves
be load bearing, as they are stretched, not compressed, and wall pressure
is directed centripetally. Only when turgor is fully mobilized against an
external resistance, and when wall tension is removed, can the tendency
for surface extension of the wall lead to the exertion of a force. By
measuring the force exerted by root tips of broad bean growing at incipient plasmolysis, Pfeffer (1893) concluded that wall growth gave rise to
forces about one-tenth as large as those produced by turgor. His experiment has not yet been repeated. One might expect that compression of
thin, flexible cell walls would lead to buckling and bending of the wall,
and changes of this kind have been described by Hottes (1929).
Where cell walls have been strengthened, continued growth of the
wall may well give rise to forces independent of those produced by turgor. Even so, the ability of thin-walled cells within an organ to withstand
compression may continue to set a limit to the pressures developed during
growth. In this connection it is worth noting that the pressures exerted
by enlarging trunks of trees, in which many of the cells have strong walls,
are comparable with those produced by delicate root tips (see Section
IV, A ) .
4. Energy Expended on External Work
We have considered contributions to plant forces that may be made
by osmotic and “active” uptake of water, by cell division, and by wall
growth. The forces observed arise most obviously from osmotically
induced turgor. Whatever contributions may or may not be made by
other processes, it is important to consider also the energy required for
external work in relation to the total energy available to the plant.
To give an example, a root of 1 mm. diameter, elongating at 1 mm.
hr.-l against a resistance of 10 bar, performs external work at the rate
of 0.2 erg sec.-l; whereas energy is released during respiration by the
root tip at rates of the order of lo2 erg sec.-l. Work may also be performed in stretching the cell wall, but again this is small ( Frey-Wyssling,
1952). It is clear that the energy expended on mechanical work during
growth is trivial compared with the output of respiratory energy, Because
of this, it is sometimes inferred that mechanical resistance is not likely
to be important. However, little is known about the efficiency with which
the plant “engine” performs mechanical work. Moreover, even if sufficient energy is available, growth may be altogether prevented by a
sufficient resistance, as there is a definite upper limit to the force that a
plant organ can exert on its surroundings.
K. P. BARLEY AND E. L. GREACEN
Effects of Mechanical Stress on the Growth of Roots and Shoots
In Section I11 we saw that large pressures are often required to
create channels in soils. For example, in loams of modest strength the
pressure needed to lengthen a channel is of the order of 10 bar. Clearly,
root tips or emerging shoots experience large stresses as they penetrate
finely structured layers or peds of soil.
Although the study of stress-stain relations in a particular organ may
help us to interpret a growth response, we are much less concerned here
with the strains produced in a given organ when a stress is first applied,
than we are with the way in which growth proceeds after a stress has
It may sometimes be overlooked that in studying underground shoots
we are dealing with dark-grown or etiolated organs, and that conclusions
reached with shoots growing in the light may not apply. Particular care
needs to be taken in extrapolating from experiments with specialized
shoots such as tendrils, that show marked growth responses both to
contact stimuli and to tension ( Brush, 1912).
as the external normal stress acting in
In what follows we define
the direction of the longitudinal axis of a plant organ, and a,, ay as the
external normal stresses acting in the direction of the remaining Cartesian
= uy we replace them by ur, the radial stress. Although we
deal only with applied stresses we note that these are superposed on
whatever stresses arise within the plant organ.
The effects of mechanical stress on the processes of cell division, cell
enlargement, and differentiation have rarely been separated in experiments, so that it is more expedient to classify the available data according
to the nature of the applied stress. We begin by considering the influence on growth of a simple axial tension or pressure.
1 . Uniaxial Stress ( # 0,
When devising methods to push or pull a radially unconfined plant
organ, it is simpler to use shoots than root tips; a shoot offers more points
of attachment for an object transmitting a force; furthermore, many
young shoots contain collenchyma and are less readily buckled or bent
than are root tips.
The influence of tension on stem growth has been studied intensively
by physiologists for two distinct reasons. First, following claims by
Pfeffer’s school at Leipzig, considerable interest was taken at the turn
of the nineteenth century in the question of whether applied tension led
( T ~
MECHANICAL RESISTANCE OF SOIL
to the regulatory development of woody tissues in stems. Unfortunately
from our present point of view the work concerned was conducted
entirely with stems grown in the light. Although good evidence was
obtained showing that the tensile strength of certain stems increased
when grown under tension (see, for example, Bordner, 1909) results
were often contradictory, The literature on the topic has been reviewed
by Schwarz (1930). Secondly, following proposals of Heyn (1931) that
the rate of cell elongation was limited by the plasticity of the wall
material, considerable attention was given to the behavior of cellulose
fibers and samples of cell wall material under tension. For example, it
has been shown that, above a certain yield stress, strips of Nitella cell
wall creep at a rate that is roughly proportional to the applied stress
(Probine and Preston, 1962). Obviously, these studies need to be supplemented by experiments with living shoots, but, as any applied stress
disturbs the turgor relations and tissue stress initially present in a shoot,
results are difficult to interpret. Recently, Lockhart et al. (1964) avoided
this problem by working with sections of pea hypocotyl incubated in a
slightly hypotonic solution, and found that the living sections underwent
irreversible extension in response to tensions greater than 50 g.wt. ( u zz
-2 bar). Such studies are of considerable interest in relation to growth
processes, but they are of less interest in relation to emergence as the
emerging shoot is subject to axial compression rather than tension.
Before proceeding to examine the effects of compression, it is worth
noting that roots are subject to simple tension in many plants, as part of
the root proximal to the zone of elongation tends to shorten, sometimes
to a considerable degree. For example, de Vries (1879) measured extenin the primary roots of red clover, TrifoEium prutense L., as
large as -0.25 over a period of several weeks. This process helps to
anchor the plant to the ground, and young seedlings can sometimes be
drawn further into the soil.
The influence of a steady push, in the opposite sense to growth, on
the elongation of etiolated shoots has been described by Sedgley and
Barley (1963), who found that this slowed elongation. In their experiment, a load of 35 g.wt. ( uz = 0.5 bar) was applied to the top of the
plumular hook of etiolated epicotyls of tick bean. The reduction in elongation rate that followed was due to a change in shape, epicotyls grown
under axial compression being wider than controls. The rate of volumetric
enlargement was unchanged. As the epicotyl of tick bean lacks an intercalary meristem, the growth response observed in this particular experiment cannot have been due to any change in cell division.
In general it is known that, where internal controls are not overriding, as in poorly differentiated dividing tissues, the direction of cell