Plant Physiol.

(1973) 51, 635-640

Mathematical Analysis of Plant Growth

ZEA MAYS PRIMARY ROOTS'
Received for publication August 17, 1972

PErER SALAMON, ALBERT LIST, JR., AND PHiLIp S. GRENETZ

Laboratory for Plant Growth Studies, Biological Sciences Department, Drexel University, Philadelphia, Pennsylvania 19104
ABSTRACT
A new mathematical treatment is given to the concept of
relative elemental growth rate, the limiting value at a point of
the relative rate of tissue growth. The new point of view requires consideration of a coordinate system in which each
point on the root surface is defined by its initial position on the
root axis. The resultant technique of plotting growth parameters provides the ability to distinguish between waves of
growth propagating toward the root tip away from cells and
waves which tend to propagate along with the cells. Thus it is
possible to model the plant growth-regulatory process in terms
of auxin and other regulators, considering both cell-associated
maxima of regulator concentration and maxima which propagate through the tissue.

Plant roots are systems whose growth is sometimes treated

as one-dimensional. As such, they represent relatively simple
growing systems, and a great deal of literature is devoted to

disregards the functional relationship between current location of points on the surface and their initial location on the
surface.
Our treatment has several advantages: whereas Erickson (2)
determined some growth parameters (relative elemental growth
rate) as a function of distance from the apex, we evaluate these
and other parameters as a function of position on the root.
Erickson, for example, chose to plot RELEL2 as a function of
distance from the tip, whereas we would like to represent it
for various points on the root (fixed cells) as a function of time,
or at any one time as a function of initial position. The data
obtained in this manner can be used to generate the plots that
Erickson's method provides. But, the converse is not true.
Thus, our treatment is more complete. We also eliminate the
assumption which Erickson and Sax (Ref. 2, p. 988) chose to
make for simplicity, that growth rate depends only on distance
from the apex. It appears to us that looking at the dependence
on time and initial distance is very important to the study of
the growth process, as Erickson (2) is well aware, and we present some techniques for looking at the dependence on both.
The present formulation begins with the idea of divergence of
velocity with respect to trajectories. At the same time, it retains
the dependence of cell position on initial position and elapsed
time. Finally, we feel that we can help to avert a number of
problems in the area of growth studies by improving the notation.
The more complete formulation presented here requires a
more sophisticated data retrieval system such as that of List

their study. The mathematical technique used in the literature

is due primarily to Richards and Kavanagh (5). Their model
enables the experimenter to notice and to focus his attention
on regional differences in growth rate. In the paper by Richards
and Kavanagh, the growth of a leaf is described in much more
detail than previous studies had been able to do. They meas- (4).
ured the extent to which different regions contributed to the
THE FORMULATION
growth process and how this might have accounted for the
final shape of the leaf. More recently, Erickson (1) has done a
If we observe the motion of a single point on the root, we
detailed study of the Xanthium leaf using improved experimen- obtain the distance of the point from the base as a function
tal and data retrieval techniques, coupled with numerical tech- of time (see Ref. 4). If we do this for several points, we obtain
niques and computer processing.
different functions of time, indeed, one for each initial position
A major step toward understanding the growth process (Fig. 1). Thus we are really dealing with a function of two
would be to explain the observed growth distribution; that is, variables: time and initial position. We designate this function
we need to determine what physiological factors are responsi- by X(x, t), where the value of the function represents distance
ble for controlling growth. Success on this front has been from the base (at time t) of a point which was initially at a
limited, but we feel that detailed growth data can provide some distance x from the base; that is, X(x, 0) = x.
remedies.
It is important to view X as a genuine function of two variaOur contention is that a slightly more sophisticated formula- bles and to examine its characteristics as such. First, how does
tion than that of Richards and Kavanagh (5) is required be- the function behave if we hold x constant? This means watchcause their approach does not make the connection between a ing the time behavior of a single point P,O whose initial distance
coordinate system fixed in space and the location of points on from the base is x0 (Fig. 2). Thus, X(x0, t) (x0 constant) gives
the expanding surface. Erickson's (2) is similar to ours, but it us the length of the segment from the base to the point P2,
as a function of time. The derivative of this function of t (the
'This work was supported by National Science Foundation
Grant GB24957 and previous Grant GB7215, to Dr. A. List, Jr.
635

2 Abbreviation:

RELEL: relative elemental growth rate.

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SALAMON, LIST, AND GRENETZ

636

'~

Plant Physiol. Vol. 51, 1973

to looking at the distances of points from the base at the single

instant to as a function of initial distance x. Thus, x is the initial
distance to the base, and X(x, to) is the distance of that same
point to time units later. The derivative of this function that
one gets by holding t constant at to is aX/a x which we call the
stretch ratio. To understand the significance of the stretch
ratio, we notice that it is the limiting value of:

X(x2, to)
X9

TIME
FIG. 1. Trajectories of three points on the primary root of Zea
mays shown at three successive points in time. In programming, a
point such as x1 is taken to be the origin.
--

X(x, to)
Xl

(asX

X9'

XI)

which is the expanded distance divided by the original distance (Fig. 4). Ergo the name stretch ratio.
We now pause and compare our results and definitions with
the classical ones by Richards and Kavanagh (5) and Erickson
(2). The most significant difference is the fact that we retained
X as a function of two variables instead of dropping the dependence on initial position. Retaining this dependence ties
together the motion of the particles instead of having separate
functions, all of them designated by the same ambiguous symbol X(t) (see Ref. 2). In Richards and Kavanagh (5) their dependence on x (the initial distance) was eliminated by "Henceforth we shall consider them as functions of the coordinate
(x, y, z) at the instant under consideration [italics added] rather
than the coordinates of the reference stage."
Equivalent terms in the old and new systems are given in
Table I. RELEL is, in our opinion, the most important index
of the growth process. In any detailed examination of growth,
one would like to say how intense the growth process is at each
point. We feel that the distribution of this "intensity" would
reveal something about the growth process. This distribution is
directly coupled to a supporting metabolism, and thus we must

TIME
FIG. 2. Displacement with time of a fixed point on the root axis.
Its location on the root is shown at two points in time.

X(x3,t0)

X(x2,to)

TIME
FIG. 4. Distance between two fixed points
function of time.

on

the root axis

as a

Table I. A Comparisont of Old anid New Growth Expressionis

Old

New

dX

ax

X(x1,to)

Xil
t

tto

=o

T IME
FIG. 3. Distribution of X as a function of
to as compared with the distribution at t = 0.

with constant t

one we get by holding x constant) is bX/l t and it represents

the rate of change of the length of the segment from the base
to P-00. In the literature this is called the growth rate.
We now examine the behavior of X(x, to) which is determined by holding t constant, equal to to (Fig. 3). This amounts

Growth rate

Relative (or "specific")

growth rate
Stretch ratio

Elemental growth rate

(RELEL)

-t

dt

1 dX

1 bx

X dt

X ot

ax
d (dX
8X aX
dX kdt Jxot /ox

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Copyright 1973 American Society of Plant Biologists. All rights reserved.

Plant Physiol. Vol.

51,

MATHEMATICAL ANALYSIS OF PLANT GROWTH

1973

examine it very carefully if we are ever to obtain an understanding of the growth process. We might even obtain some
clues to the nature of the underlying physiological patterns
which determine form.
The intensity of growth at each point is the rate of increase
in length per unit length. The length of the segment between
P., and P,2 is X(x2,. t) - X(x1, t). The time rate of change of
this length per unit length is then

a
t)
at (X(x2,
X(x2, t)

RELEL

mrrVmm-hr
.66

X(X,, t))
.51

X(X1, t)

637

RELEL is a measure of growth intensity at a point and is the

limiting value of the above expression as we take smaller segments (by using points closer to each other initially).

.36
.21

RELEL

xi

-)

(X(2, t) - X(b, t)
X(X2, t) X(XI,t)

.06

.
-009
00 1.5 3.0 45 6.0 7.5 9.0 10.5 120 135 15.0 mm

(at X(x2, t) -aX(x,

t)t

Li

CURRENT DISTANCE FROM ROOT TIP

FIG. 5. Relative elemental growth rate as derived by an earlier
numerical method plotted at a sequence of times against X, current
position, as opposed to x, initial position.

X2 - X1 l

a2X /lax

axat /

ax

which gives RELEL in terms of the partial derivatives of X.

It also allows us a further interpretation of RELEL. By a well
known result from several variable calculus, if a function is
smooth (has continuous second partial derivatives) the order
of partial differentiation does not matter, so that,
RELEL

Tipward Displacement
Stable Cel Associated Maximum/

/ax/ ax

-I- ax/ ax

at
a

at

(ln-Iax\

(1)

ax/

-J
LUJ

13:

Thus, RELEL is the time rate of change of the stretch ratio

divided by the stretch ratio; that is, the relative (specific) rate
of change of the stretch ratio. Equation 1 is very convenient
for use in integrating RELEL to recover X(x, t).
x (Initial Distance)
IMPLICATIONS
If we wish to relate growth parameters to physiological factors, we have to follow what happens to values of these paFIG. 6. Hypothetical distribution of RELEL at four successive
rameters with time at specific points fixed in the plant and not
at points fixed in space. In Erickson and Sax's studies (2) times (with time proceeding from the lowest curve to the highest).
RELEL is plotted as a function of distance from the apex, and Intended to indicate the possibility of stable cell-associated maxima
since different cells will be at that fixed distance from the apex as distinct from the large tipward displacing maximum.
at different times, this allows no way to follow a single cell and
observe its growth behavior. Data from our laboratories sug- sylvania under a United States Public Health Service traineegest that the behavior of RELEL is bell-shaped in x and t, with ship (1965-66).
The natural question to ask in studying the displacement of
superimposed oscillations in x. We think that a closer examination of these preliminary results would yield information on these waves is how the rate of their displacement compares to
physiological reasons for this behavior. For instance, Erickson the rate of movement of cells on the root. If the waves acand Sax (2) noted an "apparent periodic nature" in RELEL as company each cell, we would be led to postulate that an effeca function of distance from the apex. Hitherto unpublished tor substance induces an initial "charge" of enzymes involved
results from our laboratories, shown here in Figure 5, represent in growth in the apical meristem and that the ontogeny folan attempt to follow the evolution with time of this spatial lowed thereafter does not depend on gradients of effector subperiodicity. The data were originally taken by List from root stance distributed along the root (Fig. 6). In that case the waves
photographs in Erickson's laboratory at University of Penn- reflect periodicities in effector concentrations at the induction

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SALAMON, LIST, AND GRENETZ

638

TIMEo
FIG. 7. Hypothetical time-course for RELEL of
from tip to base.

point moving

site. If the waves travel relative to the cells, we would postulate

that effector molecules or some other modulator substance is
moving relative to the cells. The direction and rate of such
movement might help to reveal the identity of the effector
substance. For example, a recent paper (6) claims an acropetal
movement of auxin in the root. Should the rate of auxin movement match the rate of displacement of our waves, this would
be evidence that the auxin or some similar effector, is, at least
in part, responsible for variations in RELEL.
To see the motion of these waves relative to cells we have to
plot RELEL versus x, the original distance, and observe what
happens at various times. RELEL also seems to follow a fairly
predictable path in time: it starts out small, reaches a peak, and
goes back down to zero in a fashion analogous to the time dependence of the concentrations of many biological substances
(Fig. 7).
Currently, an attempt is being made to obtain analytical expressions for RELEL based on theoretical consideration of
physiological processes. We postulate a model of growth control and obtain therefrom an analytical expression for RELEL.
Upon integration, this expression yields growth curves which
may be compared with observed growth data from streak
photographs

to test

the model. If
a

RELEL

o x\

lnI
=g(x, t)
ax/

at

then
ax

It

exp

and

g(x, s) ds)

so

X(x, t)

g(y, s)

fexp

ds)

dy

integrals can be evaluated numerically or

analytically, depending on the nature of g(x, t). Given RELEL
as g(x, t) and letting l(t) be the length of the root at time t,

where the indicated

I(t)

X(10, t)

exp (

g(y, s)ds) dy

1(0) is the initial coordinate of a fixed point in the

lo region
of the root.

where =
mature

METHODS

While the general method for obtaining the streak photodata and processing them has been described in an
earlier paper by one of us (4), there have been certain refinements in: (a) the experimental technique, (b) computer processing, and (c) data retrieval. Although these improvements

graph

Plant Physiol. Vol.

51,

1973

will be extensively described elsewhere, we willgive a brief

summary of the conditions for the experiment and the method
of data handling.
Surface-sterilized caryopses of a vigorous Zea mays hybrid
were pregrown in a dark germinating chamber at 25 C and
50% relative humidity until the primary roots reached a length
of 4 to 5 cm. Selected seedlings whose roots and shoots were
particularly vigorous were transplanted to the quartz glass flow
guides with the primary root surrounded by flowing mineral
nutrient solution (4), saturated with 02, and the caryopsis was
kept moist with a cotton wick. Streak photographs were produced as before but using relatively nonactinic green light,
rather than red light. The roots were allowed to grow undisturbed for several hours prior to photography, with growth

patterns becoming quite smooth. Transients resulting from

mechanical disturbances had died out by this time.
Raw data taken by the coordinate digitizer-key punch combination is not presented in tabular form. but exists on hundreds of punch cards. However, the image of the raw data is
shown in Figures 8A and 8B as graphic output printed by a
Calcomp plotter with high precision. An earlier graph (displaying some work done at the University of Pennsylvania),
Figure 5, was plotted by the line printer, one curve per set of
coordinates. The separate curves were then traced by hand
onto the same set of coordinates with each curve subjected to
an increment of upwards displacement to represent the progress of time.
In the newly processed data (obtained at Drexel University)
(Figs. 8A-8H), the same incremental displacement technique
was used on the graphic output to represent time (Figs. 8A,
8C, 8E, and 8G), or to represent distance (Figs. 8B, 8D, 8F,
and 8H). A new computer program was devised by Grenetz to
calculate numerically the various growth expressions and to
cause the plotter to record them graphically. This program employs minimal smoothing with five-point. 1st degree, least
squares line fitting to unequally spaced data points along the
distance axis, but with equally spaced sampling on the time
axis. All curve fitting is done with the same five-point. 1st degree routine, and all derivatives represent the slopes of these
line segments. Each fitted line segment serves only to provide
one derivative, or one function value, at the midpoint of each
raw data
five-point segment, in transformed versions of the processing
(Figs. 8C-8H). A library of subroutines for the data
has taken 3 years to develop, and higher degree curve fitting
has been applied with nearly identical results. A new program
employing polynomial interpolation requiring equally spaced
input data is also being planned, which may provide much
needed error bounds. The details of such data processing are
extremely space-consuming to describe but are an important
part of this kind of growth research.
PRELIMINARY OBSERVATIONS
A streak photograph of a recent experiment using an improved apparatus (List, Grenetz, and Peacock, in preparation)
was scanned with the coordinate digitizer (4). The photograph
was projected onto a grid of parallel lines to aid in sampling
data at equally spaced time intervals of 6 min duration. A se-

as to
quence of closely spaced streaks (Fig. 8B) was selected so Startprovide adequate information in the zone of elongation.
the first
ing from a basal point on the root axis at time t = 0,root
axis
sequence of points selected for scanning along the
are designated as the "initial distances," small x, in the theory
section of the paper.
A new program prepared by one of us (P. Grenetz) was
used to compute and plot various growth parameters (see
Table I), including the raw data. These plots are shown in

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Copyright 1973 American Society of Plant Biologists. All rights reserved.

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9)

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639
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640

SALAMON, LIST, AND GRENETZ

Figures 8A through 8H. Figures 8A, 8C, 8E, and 8G portray

the growth parameters as functions of position on the root
at various times. Figures 8B, 8D, 8F, and 8H represent growth
parameters as functions of time for various points on the root.
(To see how these figures were obtained, see methods section.)
Figures 8E and 8G are intended to answer one very important question posed earlier in this paper: Do secondary maxima
and minima of growth propagate along the root at the same
rate as, or at a different rate from, that of displacing cells?
Since the size of the zone of maximal elongation, with respect
to a spatial coordinate system, tends generally to remain constant over time, its apparent size with respect to the initial
position coordinate system diminishes with time. This is obviously so because some of the original points are displaced out
of the zone of elongation as time proceeds. Also, since the
distance between the tip and the zone of maximal elongation
tends generally to remain constant, this distance with respect
to the initial position coordinate system diminishes with time.
Thus, the primary maximum of RELEL contracts and
propagates tipward approaching a constant distance from the
tip, on our graph, Figure 8G.
The value of the present approach lies in the possibility of
separating the propagation of waves traveling relative to cells
from the motion of waves which travel along with the cells.
The stretch ratio as a function of x represents the distribution of cumulative fractional expansion along the root. The
same phenomenon of displacement toward the tip applies to
the primary maximum of this distribution as well as that of
RELEL. Adjustment of smoothing and sampled data spacing
will yield more information about the motion of secondary
extrema suggested by Figures 8E and 8G.
It will be noted in Figure 8F that as one proceeds toward
the zone of maximal elongation, the form of the stretch ratio
versus time curve evolves from concave to convex. Beyond
this zone a sharp return is made to curves of low, fairly constant slope. These curves represent points near the cell division
zone which have not yet made their rather abrupt transition

Plant Physiol. Vol. 51, 1973

into the elongation zone. A little reflection reveals that the

curves of Figure 8F represent cells in different phases of their
ontogeny. If the entire ontogenetic sequence could be seen for
a single cell, the form of the curve would be sigmoidal with a
long period of time spent in the stage of upward curvature and
a rather abrupt inflection as the cell is displaced from the
elongation zone into the basal region.
With regard to Figure 8H, recall the bell-shaped curve of
Figure 7. Here we have portions of this bell-shaped curve for
RELEL at various points selected along the root axis. The
shape will be more pronounced when data spanning a larger
time interval are processed.
CONCLUSION

Currently, an attempt is being made to obtain analytical

expressions for RELEL based on theoretical consideration of
physiological processes. We postulate a model of growth control and obtain therefrom an analytical expression for RELEL.
Upon integration, this expression yields growth curves which
may be compared with observed growth data from streak
photographs to test the model.
LITERATURE CITED

1. ERICKSON-, R. 0. 1966. Relative elemental rates and anisotropy of growth in

area: a computer programme. J. Exp. Bot. 17: 390-403.
2. ERICKSON, R. 0. AND K. SAX. 1956. Elemental growth rate of the primary root
of Zea mays. Proc. Amer. Phil. Soc. 100: 487-498.
3. HEJNOWICZ, Z. 1961. The response of the different parts of the cell elongation
zone in root to external ,/-indolylacetic acid. Acta Soc. Bot. Pol. 30: 25-42.
4. LIST, A., JR. 1969. Transient growth responses of the primary roots of Zea
mays. Planta 87: 1-19.
5. RICHARDS, 0. W. AND A. J. KAVANAGH. 1943. The analysis of the relative
growth gradients and changing form of growing organisms. Amer. Natur. 77:
385-399.
6. WILKIN-S, M. B., A. R. CANE, AND I. MICCORQUODALE. 1972. Auxin transport in
roots. VII. Uptake and mov-ement of radioactivity from IAA-14C by Zea
roots. Planta 105: 93-113.

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Copyright 1973 American Society of Plant Biologists. All rights reserved.