Annals of Botany 77 : 179–185, 1996
Resource Capture by Localized Root Proliferation : Why Do Plants Bother ?
DAVID ROBINSON
Cellular and EnŠironmental Physiology Department, Scottish Crop Research Institute, Dundee DD2 5DA, UK
Received : 7 July 1995
Accepted : 6 October 1995
Using data from a well-known, published experiment [Drew (1975) The New Phytologist 75 : 479–490], the potential
exploitation of locally available nutrients by barley roots is calculated. Local proliferation of lateral roots does not
necessarily achieve significantly greater exploitation of mobile soil resources like nitrate, but it does for less mobile
ones such as phosphate. Despite this, the magnitude of the proliferative response is as great to locally available nitrate
as it is to phosphate. This implies an ‘ over-production ’ of roots in response to localized nitrate availability, prompting
a re-evaluation of the nature and implications of the response mechanism(s) of roots to soil heterogeneity.
# 1996 Annals of Botany Company
Key words : Hordeum Šulgare, barley, carbon, heterogeneity, lateral root, nitrate, localized nutrient supply, phosphate,
proliferation, root.
INTRODUCTION
The responses of plant roots to the localized availability of
soil resources are widely documented. They are a central
feature of current thinking about how plants cope with
environmental heterogeneity (Caldwell and Pearcy, 1994 ;
Hutchings and de Kroon, 1994). Species’ responses to
locally available nutrients can differ quantitatively. But,
typically, roots proliferate in regions where nutrients are
most concentrated and avoid those where nutrients are in
short supply (Robinson, 1994 a). The same is true for water
(Gallardo, Turner and Ludwig, 1994). This is regarded as an
obvious mechanism whereby plants compensate for the
variability of soil.
At the same time, plants have been considered by many
authors (e.g. Givnish, 1986 ; Robinson, 1986 ; KastnerMaresch and Mooney, 1994) to partition their captured
resources (including carbon) optimally, achieving maximal
returns at minimal cost. Plants less adept than others in this
resource balancing act are presumed to be at greater risk of
elimination by natural selection. Although never tested
experimentally, this remains an implicit justification for
many mathematical probings in plant ecophysiology (see
Gleeson and Tilman, 1992). If this presumption is correct,
plants should respond to locally available nutrients only as
long as they obtain a net benefit from so doing. Otherwise,
they would be wasteful, partitioning resources nonoptimally : ‘‘… viewing the plant as an ‘ optimal forager ’ can
lead to the prediction that in nature plants should vary in
physiology and morphology so as to avoid excess foraging
for a nonlimiting resource and to maximize effort expended
in the acquisition of a limiting resource … The most efficient
allocation of foraging effort and thus the greatest fitness for
an individual plant result in a morphology and physiology
for which no resource is taken up in excess …’’ (Gleeson and
Tilman, 1992).
To test this idea, I have analysed data obtained in a well0305-7364}96}020179­07 $12.00}0
known, published experiment on barley (Drew, 1975). In
addition, data collated by Robinson (1994 a) have been
further analysed to examine the generality of the conclusions
reached from the barley experiment.
EXPERIMENTAL METHODS
Full details and data are given by Drew (1975). Briefly,
barley (Hordeum Šulgare cv. Proctor) seedlings were grown
in pots of irrigated sand. The pots were divided into three
hydraulically isolated compartments, top (A), middle (B)
and bottom (C). The compartments were separated by wax
membranes through which the five seminal axes of each
plant could grow, but not laterals. The top two compartments were 4 cm deep, the bottom, 30 cm. Each pot was
6±8 cm in diameter. The top two compartments each had a
volume of 145 cm$. Each compartment was irrigated
separately with a nutrient solution at a rate of about
2 cm$ min−". Two treatments will be considered here. In the
controls, all three compartments received the full nutrient
solution. In the localized nutrient treatment, only the middle
compartment, B, received the full solution. The top and
bottom compartments, A and C, were supplied with a
solution containing one nutrient (P, NO−, NH+ or K) much
$
%
more dilute than the rest. This had the effect of localizing
each nutrient to compartment B. Plants were grown for
21 d, when they were harvested. Dry weights of shoots and
roots were measured, as were the lengths of axes and lateral
roots in each compartment.
Localizing the supplies of P, NO− or NH+ to the middle
$
%
compartment resulted in proliferations of lateral roots in
that compartment, and their suppression in compartments
A and C, relative to the controls [see fig. 4 in Drew (1975) ;
Table 1]. No proliferation or suppression was caused by
supplying K locally. Analysis of variance of Drew’s data
showed that there were no significant differences between
# 1996 Annals of Botany Company
180
Robinson—Localized Resource Capture
T     1. Root length (m per plant) of barley grown for 21 d
with uniformly aŠailable nutrients (control ) or with P or NO−
$
supplied only to roots in compartment B, as described in the
Experimental Methods section. Data are deriŠed from Table
3 of Drew (1975) and M. C. Drew (pers. comm., 1988). Data
for first and second order laterals are combined
Locally supplied
Root type
Axis
Lateral
Axis­lateral
Pot
compartment
A
B
C
Total
A
B
C
Total
A
B
C
Total
Control
P
NO−
0±2
0±2
1±5
1±9
18±5
22±1
16±2
56±8
18±7
22±3
17±7
58±7
0±2
0±2
1±7
2±1
2±2
37±1
7±3
46±6
2±4
37±3
9±0
48±7
0±2
0±2
1±8
2±2
1±4
40±0
2±4
43±8
1±6
40±2
4±2
46±0
$
the relative responses of roots to localized P or NO−. Plants
$
grown with locally supplied P had the same total dry weight
as the controls ; those in the other treatments were only
71–85 % as heavy.
THEORETICAL METHODS
General
The purpose of this section is to calculate the extent to
which roots in the middle compartment in Drew’s (1975)
experiment could have exploited the locally available
nutrients P and NO−. This was done using the data for root
$
growth reported by Drew and by assuming reasonable
diffusivities of P and NO−. Theoretically, all ions have
$
similar diffusivities in saturated sand (as used in Drew’s
experiment), although no experimental evidence for this
appears to exist. In soil, however, ion diffusivities are very
different, and it is when these differences in mobility among
ions occur that the localized growth responses of roots are
most likely to be important in nutrient capture. NO− is
$
relatively mobile in moist soil ; P, because of its exchange
reactions with charged surfaces, diffuses more slowly (Clarke
and Barley, 1968 ; Nye and Tinker, 1977, p. 71). The other
ions that Drew studied, NH+ and K, are of intermediate
%
mobility. The analysis presented here, therefore, examines
the consequences of the responses measured by Drew had
they occurred in soil rather than irrigated sand.
Exploitation was estimated as the fraction of the locally
supplied volume (compartment B of Drew’s pots) from
which roots could have withdrawn P or NO−, following
$
Fitter (1987) and Berntson (1994). This fraction is the sum
of the volumes of the concentration depletion zones around
the roots (Nye and Tinker, 1977, p. 130) and those of the
roots themselves, divided by the volume of space in which
those roots were growing. When the ‘ exploited ’ volume
equals the volume of space containing the roots, any further
root growth would give the plant access to relatively little
more nutrient. This does not imply that the roots would
necessarily have absorbed all the nutrients available to
them, only that they would have the potential to do so.
This analysis was done in four steps. (1) Calculate the
lengths of seminal axes and laterals on day 21 of Drew’s
experiment. (2) Calculate root growth rates in compartment
B between days 0 and 21, assuming linear and exponential
rates of change in the lengths of axes and laterals,
respectively. (3) Calculate root radii from Drew’s measurements of root dry weight and the lengths calculated in (1).
(4) Calculate the volumes of the depletion zones of P and
NO− around the roots in compartment B of locally supplied
$
plants.
Steps 1–3 were done for control and locally supplied
plants ; step 4, for locally supplied plants only. Details of
these procedures now follow so that the route from Drew’s
original data to the quantities derived from them is as
transparent as possible. All symbols are defined in the
Appendix.
Root lengths at day 21
Seminal axes. Drew reported the length of each root axis,
a (cm). The total length of root axis per plant, A, is simply
A ¯ na
(1)
where n is the number of axes per plant (five).
It is assumed that axes grow vertically downward.
Consequently, the maximum length of an axis in compartments A or B is the depth of that compartment, z (4 cm)
and is given by
(2)
AA,B ¯ nz
The length of axis in compartment C is then found by
difference :
(3)
Ac ¯ A®2AA,B
Laterals. Drew reported values of Ii, the lengths of
laterals (first plus second order) per cm of seminal axis in
each compartment, i, of the pot. Thus, the total length of
laterals, Li, in patient i is the product of I and the length of
axis per compartment :
Li ¯ Ii Ai
(4)
Equations (1)–(4) were used to derive the data shown in
Table 1 on which subsequent calculations were based.
Root growth rates
Seminal axes. It is assumed that axes extend at a constant,
linear rate, R (cm d−"). At any time, t (d), therefore, the
length of axis per plant is given by
A(t) ¯ Rt
(5)
Values of A measured on day 21 (Table 1) were used to find
181
Robinson—Localized Resource Capture
T     2. Parameter Šalues obtained as described in the Theoretical Methods section
Locally supplied
Parameter
Symbol
Rate of change of axis length
R
Time for axes to enter compartment B
Rate of change of lateral length in B
Specific root length
Mean root radius
Ion diffusion coefficient
tB
r
λ
o
D
per plant
per axis
large
small
R for control and locally supplied plants (Table 2). These
values seem reasonable. Rose (1983) quoted 2 cm d−" per
axis of barley in nutrient solution.
The time, tB, at which the axes entered compartment B is
given by
(6)
tB ¯ zInR
Laterals. It is assumed that the length of laterals in
compartment B, LB, increased exponentially from the
moment that axes entered from compartment A. An
equation that describes this behaviour is
LB(t) ¯ exp[r(t®tB)]®1
(7)
d−").
where r is the rate of change in lateral length (cm
[The
®1 in eqn (7) ensures that at t®tB ¯ 0, L ¯ 0 also.]
Equation (7) implies a linear increase in the logarithm of
root length. Robinson and Rorison (1983) found such an
increase for the roots of three grass species receiving
localized supplies of N in nutrient solution. The dry weight
of barley roots supplied locally with P showed the same
trend (Drew and Saker, 1978). As before, r was found using
values of LB measured on day 21 (Table 1) ; these are given
in Table 2.
Total root length in compartment B.
Total root length in compartment B at any time, t, is the
sum of the lengths of axes and laterals in that compartment :
TB(t) ¯ AB(t)­LB(t)
(8)
Equation (8) was used to generate daily cohorts of root
length from which ion depletion zones were calculated (see
below). The total length of roots in a cohort produced in
compartment B on day t is the difference between the
lengths on successive days, i.e.
χB(t) ¯ TB(t)®TB(t®1)
(9)
Root radii
Drew did not report root radii. As a best approximation,
mean radii, o (cm), were calculated from cylindrical
geometry and Drew’s measurements of root dry weight and
length by
(10)
o ¯ 1}oπλφρ
where λ is the ratio of root length (cm) and dry weight (g),
the specific root length, in other words (Table 2). ρ is the
Units
Control
P
NO−
cm d−"
cm d−"
d
cm d−"
cm g−"
cm
cm# s−"
cm# d−"
cm# s−"
cm# d−"
9±05
1±81
2±21
0±410
0±044
0±008
9±86
1±97
2±03
0±433
0±055
0±008
5¬10−)
0±004
5¬10−*
0±0004
10±22
2±04
1±96
0±435
0±040
0±009
5¬10−'
0±432
5¬10−(
0±043
$
specific gravity of root tissue (assumed to be 1 g cm−$), and
φ is the dry weight : fresh weight ratio of root tissue
(assumed to be 0±1). Values of o produced by eqn (10) are
shown in Table 2 ; these varied little among treatments.
Ion depletion zones
The radius of the notional outer boundary of a depletion
zone, x (cm), of an ion diffusing to a cylindrical sink, the
root, in a porous medium can be approximated by (Nye and
Tinker, 1977, p. 231) :
x(τ) ¯ o­2oDτ
(11)
τ is the time (d) since the cohort of roots was produced, and
since they started exploiting nutrients, and distinct from t,
the time since the start of the experiment. In other words, τ
is t®t where t is the time when the roots were produced.
!
!
Equation (11) calculates the root-mean-square displacement
of a diffusing substance (Nye and Tinker, 1977, p. 136).
Statistically, some of the substance will have moved from a
distance greater than x cm after τ s. So, eqn (11) calculates
an ‘ average ’ radius of depletion. Moreover, eqn (11) applies
strictly to diffusion to a planar sink rather than to a
cylinder. Comparing eqn (11) with a more exact equation
published recently by Syring and Claassen (1995) gave,
however, a mean discrepancy between the two of only
³16 %, depending on time and diffusivity.
D is the ion’s diffusion coefficient in soil (cm# d−"),
assumed constant. Rather than assume a single value, it was
felt safer to assume a large and small D for each ion. This
allowed upper and lower limits to be put on the volumes
exploited. For NO−, Clarke and Barley (1968) reported D in
$
a moist sandy soil of 5¬10−' cm# s−". When diffusion was
impeded by drying, D fell to one tenth of this value. These
were taken to be the large and small values of D for NO−.
$
For simplicity, I assumed that P diffused two to three orders
−
of magnitude more slowly than NO in the same system, i.e.
$
values of D of 5¬10−* to 5¬10−) cm# s−" were assumed for
P. This is a generous assumption, as the diffusivity of P in
soil has been measured to range from 10−"% to 4¬10−* cm# s−"
(data compiled by Fitter and Hay, 1987, p. 85).
Equation (11) assumes that ions are absorbed as soon as
roots are produced. It also assumes that roots suffer no
physiological impairment or developmental change that
182
Robinson—Localized Resource Capture
Š(t) ¯ π[x(τ)]#χB(t)
(12)
Therefore, the total volume, V(t) (cm$), of the depletion
zone up to time t is the sum of the volumes around each
cohort produced up to that time :
t
V(t) ¯ 3 Š(t)
(13)
tB
Values of V(t) were calculated until V " 145 cm$, the
volume of compartment B, or until t " 21 d, the duration of
the experiment.
RESULTS
The time-courses of exploitation of the middle compartment,
B, in Drew’s (1975) experiment are shown in Fig. 1. For
NO−, full exploitation occurred after only 4±5–11±5 d,
$
depending on the mobility of the ion. Full exploitation of P
was also probable after 18 d, but only if a large diffusion
Fractional exploitation
1
0.8
0.6
0.4
0.2
0
3
6
9
12
Time (days)
15
18
1
Fractional exploitation
might limit absorption. This is a reasonable assumption for
the time-scale of Drew’s experiment and for the young
cereal plants he used. Equation (11) also implies no overlap
of adjacent depletion zones until the soil becomes fully
exploited. Overlap could be included only with a more
sophisticated mathematical description of the growth of the
root system. That of Rose (1983) would be particularly
useful as it was based partly on data obtained for barley
root systems, but ones grown in nutrionally uniform nutrient
solution rather than non-uniform sand. Different forms of
the equations used here would generate different timecourses of exploitation. This is a point of detail that would
require even more assumptions (both conceptual and
numerical) that Drew’s (1975) data cannot (and were not
designed to) support.
The volume, Š(t) (cm$), of the depletion zone formed
around each cohort of roots in compartment B at any time
since the cohort was produced is :
0.8
0.6
0.4
0.2
0
3
6
9
12
Time (days)
15
18
21
F. 2. As for Fig. 1, but assuming that root growth in response to
locally available NO− or P was the same as in control plants receiving
$
uniformly concentrated supplies of nutrients.
coefficient was assumed. With the smaller value of D, only
33 % of full exploitation of P was possible by the end of the
experiment.
We now ask : what would have happened had no
proliferation greater than that in the control occurred in the
middle compartment ? This question was addressed by
replacing LB in eqn (8), for both P and NO−, with the length
$
of laterals measured in compartment B of the controls. This
generated the same, smaller value of r for both treatments
(Table 2). The result is in Fig. 2. The time-courses of
exploitation of NO− would have barely differed from those
$
in Fig. 1. Full exploitation of NO− would have been delayed
$
by only 0±5 d compared with Fig. 1. That of P would have
been delayed by up to 1 d. With the smaller D, only 21 % of
full exploitation would have been possible after 21 d without
the localized proliferation of roots.
Taking this line of thought to its logical conclusion we can
now ask, What would have happened had no laterals been
produced in compartment B ? The plant would then have
had to exploit the nutrients in the middle compartment via
only its five seminal axes. This question was addressed by
simply assigning a value of zero to LB in eqn (8).
This biologically improbable event would have had no
effect on the exploitation of NO− if D was large (Fig. 3). Full
$
exploitation would have been delayed by up to 3 d,
compared with Fig. 1, with a small diffusivity. For P,
however, the complete absence of laterals would have been
disastrous, with hardly any exploitation possible, whatever
value of D was assumed. Only a maximum of 13 % of full
exploitation would have been possible with a large D, and
one-tenth of this with the smaller D.
21
F. 1. The fraction of the locally available nutrient exploited by barley
roots in Drew’s (1975) experiment, calculated using eqn (1), as
described in the text. (——) NO− ; (– – – – – –) P. The upper curve for
$
each nutrient is calculated using the larger diffusivity given in the text
and Table 2 ; the lower with the smaller diffusivity. The time axis refers
to the number of days’ growth of the barley seedlings.
DISCUSSION
The impact of localized root proliferation on local
exploitation of P and NO−
$
The necessity for the production of extra lateral roots to
exploit supplies of locally available P is clear from Fig. 1.
Robinson—Localized Resource Capture
obtained from data collated by Robinson (1994 a). These
data were from many published experiments in which
control plants received uniformly enriched supplies in
nutrients, as in Drew (1975). On average, therefore, roots do
not respond morphologically any less to locally available
NO− than they do to P. This, and the results shown in Figs
$
1–3, suggests that responses to locally available NO− are
$
likely to be superfluous for effecting the capture of that
−
NO .
$
What is the reason for this ? Without firm details of the
underlying physiological mechanisms, the best answer one
can give is to offer arguments for various possible
explanations in the hope that they stimulate deeper inquiries.
Fractional exploitation
1
0.8
0.6
0.4
0.2
0
3
6
9
12
Time (days)
15
18
21
F. 3. As for Fig. 1, but assuming no production of lateral roots in
either treatment.
T     3. The size, as a percentage of that in uniformly
supplied controls, of roots locally supplied with or depriŠed of
NO− or P. Data are from Tables 2 and 3 (for NO− and P) and
$
$
Figs 2 and 3 (for P only) of Drew (1975) for barley, and
compiled from numerous original sources by Robinson (1994a)
Reference
Drew (1975)
Robinson (1994 a)
183
Nutrient
NO−
$
P
P
NO−
$
P
P
Roots supplied
with nutrient
Roots deprived
of nutrient
135
181
0±11, n.s.
158
198
0±28, n.s.
49
58
0±84, n.s.
61
65
0±65, n.s.
‘ Size ’ was measured as dry weight, length or number. Statistics were
derived from a single factor analysis of variance on log-transformed
data ; n ¯ 3 for NO− and 7 for P (Drew, 1975) ; n ¯ 64 for NO− and 72
$
$
for P (Robinson, 1994 a).
After 21 d, root proliferation exploited up to 57 % more P
compared with the control (33 % of full exploitation in Fig.
1 ; 21 % in Fig. 2). The effect was greatest at small diffusivities
and diminished as D increased. Such a necessity for the
proliferation of lateral roots is less obvious for the
exploitation of locally available NO−. The necessity for any
$
laterals to exploit NO− is similarly obscure (Fig. 3). What is
$
clear is that axes alone are quite inadequate for effective
exploitation of P.
It takes no great insight to reach these conclusions,
predictable qualitatively since Bray (1954), so they are
hardly new findings. But from Fig. 1 and the ‘ optimality ’
principle outlined in the Introduction, one might be tempted
to predict that the response of roots to locally available NO−
$
would be smaller than that to P. This prediction does not
accord with the evidence.
Table 3 shows that there was no difference between the
root responses of barley to the localized P and NO−
$
treatments in Drew’s (1975) experiment. Statistics similar to
these are also presented in Table 3 for other species,
The response is non-specific
The first possibility is that the mechanisms whereby
plants detect and respond morphologically to significant
variations in nutrient availability may not be subtle enough
to discriminate one ion from another. Any ionic imbalance,
provided that it is large enough and the plant’s demand for
the ion is big enough, may trigger effectively the same ‘ allor-nothing ’ response. That happened in Drew’s (1975)
experiment. Both NO− and P elicited an ‘ all ’ response, and
$
K nothing, at least in terms of localized root growth.
Once initiated, perhaps the proliferative response continues as a developmental ‘ cascade ’, similar to that which
leads to the hairy root syndrome when roots are infected
with the Ri plasmid from Agrobacterium rhizogenes. What
then could switch off the cascade ? Drew (1975) suggested
that the eventual exhaustion of a locally available nutrient
signals the end of further proliferation. Another way of
putting this is that proliferation stops when the spatial
imbalance in ionic activity among the regions containing the
root system is reduced below a certain threshold. The design
of Drew’s pots, with the continual renewal of nutrient
supplies, prevented this from happening. This would also
apply to the vast majority of similar experiments, done in
replenished nutrient solutions (see Robinson, 1994 a).
But in soil, a localized supply of nutrients will eventually
be exhausted by the roots, microbes, or chemical and
physical processes and could, therefore, switch off the
proliferative response. However, there is evidence that root
proliferation in soil continues after a locally available source
of nutrients is exhausted. Van Vuuren, Robinson and
Griffiths (1995) grew wheat roots through a layer of
rapidly decomposing organic matter in otherwise N-deficient
soil. Root proliferation occurred most markedly during the
last third of the experiment. Then, only negligible amounts
of NO− and NH+ were available to those roots and differed
$
%
little from the concentrations of these ions in bulk soil.
If the morphological response of roots to a locally
available supply of nutrients is so non-specific, and if it is to
ever genuinely benefit a plant expressing it, the response
must be capable of improving the exploitation of the least
mobile nutrients in soil. Then, the exploitation of more
mobile nutrients by a response of that magnitude would be
inevitable but inefficient as more roots would be produced
than would be needed. This seems to be what happens in
barley. The evolution of a non-specific response system
184
Robinson—Localized Resource Capture
sufficient to exploit only mobile resources would be useless
for the capture of less mobile ones.
Such non-specificity in response to variations in nutrient
supply does not apply to processes involved in transporting
ions into root cells. When a nutrient is localized, or withheld
for a time then re-supplied, its rate of uptake per unit of root
is stimulated (see Robinson, 1994 a, b). This effect is
generally restricted to the nutrient whose supply has been
varied ; the uptake of other, uniformly available, nutrients is
unaffected (Drew and Saker, 1978 ; Lee, 1982 ; Jager, 1985 ;
Robinson, Linehan and Gordon, 1994).
Roots operate in a multi-ion enŠironment
In soil solution, the concentrations of individual ions are
coupled electrochemically to those of all the others. Large
changes in concentration of one ion may cause simultaneous
changes in the concentration of another ion. For example,
additions of NH NO to soil releases K and P from
%
$
exchange sites, transiently increasing the concentrations of
these ions in the soil solution (Yanai et al., 1996).
If a root meets a localized concentration of an ion that is
otherwise sparsely available, it is likely that it will meet an
improved availability of other ions, too. A morphological
response capable of opportunistically exploiting such
localized variations in availability would, as discussed above,
have to be capable of capturing the least mobile nutrients to
be effective.
Roots eŠolŠed in a competitiŠe enŠironment
An individual may gain as much by reducing the resource
capture by a neighbour as it would by maximizing its own
capture of the resource. Then, the speed of full exploitation
would be an important factor, rather then the physiological
efficiency with which exploitation is achieved.
If effective, such mechanisms might be expected to evolve
in many taxa because those that did not express the
response would be more likely to be evolutionarily disadvantaged. In my survey of 41 species (Robinson, 1994 a),
all expressed some growth (or suppression of growth)
response in their roots to locally available nutrients.
Roots do not operate independently of shoots
Jager (1985) found a close association between the
concentrations of P and N in maize shoots and the growth
stimulation of roots locally supplied with P or NO−. When
$
the concentrations of P and N were restored to, respectively,
70 and 90 % of those in uniformly supplied control plants,
root proliferation in the nutrient-rich zone was suppressed.
This did not happen when K or Ca were supplied locally.
Jager found responses similar to those of maize in Plantago
major and P. lanceolata, but not P. media, when they were
supplied locally with P. Internal controls, related to the
shoot concentration of, or sink strength for, some locally
supplied nutrients may exert as strong an influence on root
development as do external factors such as ion concentration
and distribution.
Shoots may also influence roots through the supply of
carbon. Modifications to the rooting medium affect, by
unknown mechanisms (Jackson, 1993), stomatal conductances, rates of leaf expansion, and therefore, rates of
carbon gain by the plant. Localization of nutrients seems to
have a transient effect on shoot growth, but one that is felt
long after the initial response to the localization. The data
of Drew and Saker (1978), for example, suggest an
interruption in the dry weight gain of barley shoots after P
was supplied locally to the root system. The interruption
must have occurred within 3±4 d of the P being localized
(3±4 d being the time between the start of localization and
the first harvest). Relative growth rates of shoot dry weight
were subsequently similar to those of control plants (0±18 d−"
in controls and 0±17 d−" in locally supplied plants). But
shoot dry weights of locally supplied plants were ultimately
(after 29 d growth) only 81 % of those of controls.
Shoots of locally supplied plants may be smaller than
those of controls, therefore, whereas total dry weights of
root systems may be similar (Drew, 1975 ; Drew and Saker,
1978). If so, net rates of carbon export from shoots must be
greater per unit shoot dry weight in locally supplied plants
than in controls. Carbon export may also be greater per
plant, as Lambers et al. (1982) found for wheat supplied
locally with NO−. The likelihood is, therefore, of the
$
concentration (or flux density) of soluble carbon being
greater in the phloem of locally supplied roots than in
control roots. This, together with the external signal of the
locally available nutrients, may trigger (and sustain ?) lateral
root proliferation near unloading regions (cf. Oparka, Prior
and Wright, 1995).
Many models of shoot–root relationships assume that
carbon can be used as a notional currency with which to
assess the value to the plant of alternative physiological
traits (e.g. Givnish, 1986 ; Fitter, 1991). For anything to be
a currency, it must be in relatively short supply and difficult
for many individuals to secure in great quantity. The notion
that carbon meets these requirements in autotrophic plants
has recently been challenged by Thomas (1994). He put
forward the provocative view that most terrestrial plants
exist in a surfeit of fixed carbon, a legacy of the assimilatory
systems that evolved before the colonization of land. Once
on land, plants were able to capture far more carbon than
could be used to combine with the relatively meagre supplies
of N, P and other nutrients available to them from soil.
Processes that removed excess carbon from taking part in
further assimilatory activities might, therefore, occur with
little detriment to the plant’s chances of survival. ‘ Looked
at this way ’, wrote Thomas, ‘ even roots invite reinterpretation. What better way of disposing of fixed carbon
than by burying it where it cannot make more assimilatory
biomass ’ !
If Thomas is right, the use of carbon in producing
apparently superfluous roots may, despite prevailing views
of the physiological costs involved, carry only a negligible
cost evolutionarily. Traits to optimize carbon use in root
growth, for example, would then be an inconspicuous target
for natural selection and imply that the optimality principle
described in the Introduction was ill founded.
185
Robinson—Localized Resource Capture
A C K N O W L E D G E M E N TS
The Scottish Crop Research Institute is funded by the
Scottish Office Agriculture and Fisheries Department. I am
grateful to Glyn Bengough, Ian Bingham, David Clarkson,
Alastair Fitter and an anonymous referee for their stimulating comments, and to Malcolm Drew and Les Saker for
doing such superb experiments.
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APPENDIX
Symbol
φ
ρ
A
a
A, B, C
χ
D
λ
L
I
n
o
R
r
T
t
τ
tB
t
!
Š
V
x
z
Definition
Dry weight : fresh weight ratio of root
tissue
Specific gravity of root tissue
Length of root axes per plant
Length of each root axis
Subscripts, refer to compartments A, B and
C of the pots used by Drew (1975)
Total length of axes and laterals in a
cohort of roots produced on a particular
day
Ion diffusion coefficient in the rooting
medium
Specific root length
Length of lateral roots per plant
Length of lateral roots per unit length of
root axis
Number of root axes per plant
Mean root radius
Rate of change of axis length
Rate of change of lateral length in
compartment B
Total length of axes and lateral roots per
plant
Time since the start of the experiment
Time since a given cohort of roots was
produced
Time for axes to enter compartment B
Time when a certain cohort of roots is
produced
Volume of the ion depletion zone around a
particular cohort of roots
Total volume of the ion depletion zone
around all cohorts of roots at a certain
time
Radial distance (from the centre of the
root) of the notional outer boundary of
the ion depletion zone
Depth of compartments A and B
Units
g cm−$
cm
cm
cm
cm# s−"
cm g−"
cm
cm cm−"
cm
cm d−"
cm d−"
cm
d
d
d
d
cm$
cm$
cm
cm