REVIEW
New Phytol. (2000), 147, 43–53
Research review
The control of carbon acquisition by roots
J. F. F A R R A R*    D. L. J O N E S
School of Biological Sciences and School of Agricultural and Forest Sciences,
University of Wales Bangor, Bangor, Gwynedd LL57 2UW, UK
Received 7 January 2000 ; accepted 6 March 2000
     
We review four hypotheses for the control of carbon acquisition by roots, and conclude that the functional
equilibrium hypothesis can offer a good description of C acquisition by roots relative to shoots, but is deficient
mechanistically. The hypothesis that import into roots is solely dependent on export from the shoot, itself
determined by features of the shoot alone (the ‘ push ’ hypothesis), is supported by some but not all the evidence.
Similarly, the idea that root demand, a function of the root alone, determines import into it (the ‘ pull ’ hypothesis),
is consonant with some of the evidence. The fourth, general, hypothesis (the ‘ shared control ’ hypothesis) – that
acquisition of C by roots is controlled by a range of variables distributed between root and shoot – accords with
both experiment and theory. Top-down metabolic control analysis quantifies the control of C flux attributable to
root relative to source leaf. We demonstrate that two levels of mechanistic control, short-term regulation of phloem
transport and control of gene expression by compounds such as sugars, underlie distributed control. Implications
for the impact of climate change variables are briefly discussed.
Key words : functional equilibrium, metabolic control analysis, phloem, root exudation, source–sink relations.
          
                
What controls the acquisition of C by roots ? None of
the several published answers to this question is
entirely satisfactory, which is unfortunate as it is a
close approximation to the more general question :
what controls the rate of root growth ? In this short
review we examine four general and contrasting
hypotheses. First, we consider the functional equilibrium hypothesis – that root growth is the outcome
of a nutritionally based compromise with shoot
growth. Second, we contrast two simple models, one
that root growth is determined by availability of C
from the shoot (‘ push ’ hypothesis’), the other that it
is determined by demand from the root itself (‘ pull
hypothesis ’). Last, we ask if root growth is determined by disparate processes distributed throughout the plant (‘ shared control hypothesis ’).
Common to all these hypotheses, and central to
deciding between them, is a good understanding of
the fluxes of C that together result in C acquisition
by the root. We therefore begin with a brief survey
of those fluxes.
The distinction between gross and net acquisition of
C is important qualitatively and quantitatively ; we
need precision : is it net or gross allocation that is in
question ? Wherever possible we need to know about
the gross fluxes that sum to yield net values.
The dominant root C fluxes which have been
quantified are listed in Table 1 ; some examples are
given by Lambers (1987) and Farrar & Williams
(1991). To summarize many investigations, the
dominant source of gross C gain by roots is via
import in the phloem from the shoot, while the
major loss of root C is via respiration associated with
growth and ion uptake (approx. 40% of that
imported ; Farrar & Williams, 1991 ; Atkin et al.,
2000), although fluxes to symbionts are appreciable
(perhaps 15% to legume nodules and 10% to
mycorrhizas). Some minor fluxes are less well
described, such as rates of dark fixation of CO
#
(probably low) and rates of uptake of organics from
soil (probably high). Uptake of organic compounds
from the soil merits further study, as it is probably
more important than dark fixation of CO by PEP
#
carboxylase. Carbon movement in the xylem also
needs more attention (Canny, 1990). However, while
most of the major C fluxes are known, the factors and
mechanisms which control them remain poorly
understood.
*Author for correspondence (tel j44 1248 382532 ; fax j44 1248
370731 ; e-mail j.f.farrar!bangor.ac.uk).
REVIEW
44
J. F. Farrar and D. L. Jones
Table 1. Main fluxes of carbon involved in net acquisition of carbon by roots
Carbon fluxes
Fluxes not resulting
directly in gain or loss
Gain
Loss
Import in the phloem
Uptake from soil
CO fixation by PEP carboxylase
#
Respiration
Exudation of organics
Exchange of bicarbonate
Export in the xylem
To symbionts
Death of cortex or whole roots
Glucose + H+
Glucose
ATP
1
5
Glucose
ATP +Pi
3
H+
2
4
Glucose
H+
Fig. 1. Proton symport for uptake of sugars from the
rhizosphere.
Studies in which whole plants have been labelled
with "%C have shown that roots lose 1–10% of net
photosynthetically fixed C in a form other than CO
#
(Curl & Trueglove, 1986 ; Whipps, 1990). This loss
is termed rhizodeposition, and includes sloughed
cells, mucilages and low molecular weight soluble
compounds such as sugars, amino acids and organic
Phloem unloading
Short-distance transport
Cellular compartmentation
Storage
Synthesis and growth
acids (Table 2). The fingerprint of compounds
released from roots depends on the environment and
internal status of the root (Barber & Gunn, 1974 ;
Cakmak & Marschner, 1988). For example, mucilage
secretion significantly increases under mechanical
stress, whilst large amounts of organic acids are
excreted under P stress (Hoffland, 1992). Do plants
exert direct control over C loss into the soil, thereby
modifying the root environment? We address this
question under hypothesis 3 below. Rhizosphere C
flow is not just a unidirectional loss : from mechanistic studies of transport processes, it is clear that
roots can also take up organic molecules from the soil
solution (Fig 1 ; Jones & Darrah, 1993). Therefore
they might be able to control the levels of low
molecular weight components accumulating in the
rhizosphere via both loss and uptake : these mechanisms are discussed under hypothesis 3.
Hypothesis 1. Net acquisition of carbon by roots is
determined by their functional equilibrium with shoots
Typically, shoot and root growth appear to be
closely coordinated, in that neither part comes to
greatly outgrow the other. Brouwer (1983) and
Thornley (1977) produced far more precise and
fundamental statements of this commonplace observation, by positing versions of the functional
Table 2. Estimates of the loss of carbon from roots attributable to the various components of rhizodeposition
Exudate
Plant
Rate of C loss
(µg C g−" root
d. wt d−")
Lactic acid
Mucilage
Sugars
Phytosiderophores
Ethanol
Amino acids
Phenolics
Organic acids
Sloughed cells
Fatty acids
Sterols
Vitamins
Flavonoids
Growth hormones
Zea mays
Vigna unguiculata
Zea mays
Hordeum vulgare
Pisum sativum
Gossypium hirsutum
Triticum aestivum
Zea mays
Arachis hypogea
Brassica napus
Brassica napus
Zea mays
Phaseolus vulgaris
Arachis hypogaea
19 458
34 000
7880
2880
130
123
334
104
72
139
12
6
3
0n07
Rate of N loss
(µg N g−" root
d. wt d−")
Reference
0
952
0
560
0
51
—
0
9
0
0
1
0
0n04
Xia & Saglio (1992)
Horst et al. (1982)
Schonwitz & Ziegler (1982)
Ro$ mheld (1991)
Smucker & Erickson (1987)
Cakmak & Marschner (1988)
++
Kraffczyk et al. (1984)
Griffin et al. (1976)
Svenningsson et al. (1990)
++
Schonwitz & Ziegler (1982)
Hungria et al. (1991)
Reddy et al. (1989)
REVIEW
Control of carbon acquisition by roots
45
Table 3. Growth and root metabolism of barley at elevated CO
#
CO concentration (ppm)
#
Parameter
350
700
Dry weight (mg)
Root weight ratio
Rate of elongation of seminal axis (cm h−")
Number of nodal roots
Rate of lateral root production (h−")
Carbohydrate content of seminal axes (mg g−" f. wt)
Respiration of seminal axes (nmol g−" s−")
Carbohydrate content of root tips (mg g−" f. wt)
Respiration of root tips (pmol per tip s−")
154
0n31
0n12
3n4
1n1
3n2
2n7
17n3
22
222
0n31
0n18
5n8
1n8
4n0
3n9
37n9
33
Barley was grown hydroponically and harvested when 14 d old. Unpublished data of B. Collis, C. Pollock & J. F.
Farrar.
equilibrium hypothesis. In essence this states that
both shoot and root acquire different resources (e.g.
C and N, respectively), but that each needs both
resources in a relatively stable ratio. Therefore
growth of the root depends on the provision of C
from the shoot as well as its own acquisition of N, so
as it gets larger, a larger shoot is needed to provide
sufficient C. Growth of shoot and root are thus
inseparably linked by this functional equilibrium.
This hypothesis has formed the basis of successful
models (Thornley, 1977 ; Hunt et al., 1990).
The functional equilibrium hypothesis gives a
good description of how many environmental
variables affect the relative growth of root and shoot
of spaced plants (Brouwer, 1962, 1983 ; Wilson,
1988) : light, water, N and P are well explained. For
example, an N-deficient plant produces a larger root
system ; a shaded plant produces a larger shoot. This
has not been shown to work in swards. It is
unambiguous in predicting that a shortage of K+ (or
any other cation) should favour root growth, when
this is not a universal finding (Wilson, 1988). It
predicts that increased atmospheric CO will increase
#
root weight ratio ; however in some cases this ratio
remains unaltered (Table 3 ; Farrar & Gunn, 1996 ;
Gunn et al., 1999a). It does not distinguish between
species, whilst there is increasing evidence that fastgrowing species are more plastic than slow growers
(Grime, 1994). And it is striking that there are far
more tests of its predictions about weight distribution than there are about activity (say of
photosynthesis, or of N uptake) per unit weight of
tissue.
For an ecologist, the functional equilibrium
model is a successful resource-based descriptor.
Unfortunately its application to plants growing in
communities has not been attempted, although in
general it might be expected to apply (Tilman, 1988 ;
Grime, 1994). For the physiologist, the functional
equilibrium hypothesis is less satisfactory. It
describes the allocation of net weight, not gross C, so
differential losses by respiration are ignored. And
most disturbingly, it is not truly mechanistic. One
example of its limitation is that in its simpler
formulations it proposes that C is retained in the
shoot unless in excess, when it is exported to the
root ; however in reality most C is fixed in mature
leaves and exported from them, and only then
partitioned between shoot and root – so its focus on
export rather than partitioning is misleading. It does
not address the question of when or how weight or
activity will be adjusted following perturbation.
Although it states that the total capacity of a root to
take up nutrient (its weight multiplied by the average
uptake capacity per unit of weight) is conserved, it
makes no statements about how these morphological
and metabolic components are related – which alters
under what circumstance and how they are mutually
regulated.
In summary, the simple functional equilibrium
hypothesis describes many but not all situations, and
is inadequate mechanistically. We now know much
more about mechanisms by which shoot and root C
flow are regulated than when the functional equilibrium hypothesis was formulated (van der Werf &
Lambers, 1996). Clearly it will be more profitable to
develop models which are based on known
mechanisms than to pursue the functional equilibrium hypothesis.
Hypothesis 2. Root carbon acquisition is determined
by the inflow of carbon from the shoot (‘ push ’
hypothesis)
The inflow of C from the shoot is the largest C flux
in the root ; therefore it nearly completely describes
gross C acquisition. However, this hypothesis goes
further and suggests that this C flow into roots is
determined entirely by the shoot. (As respiratory C
loss by roots is a nearly constant proportion of
import, net and gross C influx are proportional.)
Root growth would then be determined by the
factors that control export from source leaves and the
shoot. The most obvious evidence supports this
hypothesis : when plants are grown in high light or
46
REVIEW
J. F. Farrar and D. L. Jones
Table 4 . Export from second leaf of barley at elevated CO : effect of sinks
#
CO concentration
#
(ppm)
Parameter
350
700
350700
700350
PN (µmol m−# s−")
CHO (g m−#)
Export of sucrose (g m−# h−")
11n2
6n1
0n93
19n0
10n4
1n73
18n2
9n6
1n58
11n8
5n3
1n22
Barley plants were grown at either 350 or 700 ppm CO and some switched () to the other CO concentration 2 d after
#
#
expansion of the second leaf. Carbohydrate content and rates of photosynthesis and export were measured 24 h later.
Export was measured by mass balance. Unpublished data of B. Collis, C. Pollock & J. F. Farrar.
high CO under nonnutrient-limiting conditions
#
their roots grow faster (Table 3 shows that roots of
barley at high CO grow more quickly by a higher
#
rate of production of lateral roots). Does the
hypothesis survive a more detailed examination?
Further on and elsewhere (Farrar, 1999a) we argue
that it does not.
What controls the rate of export from source leaves ?
The simplest hypothesis is that export from leaf and
shoot is directly determined by leaf photosynthetic
rate. Import to the root must equal the balance
between photosynthesis and storage plus growth in
the shoot ; but this description says nothing about
where control is exercised. Rather, if this hypothesis
were true there would be a continuous linear
dependence of export on photosynthesis. However
the relationship between photosynthesis and export
is easily broken, so that export must be regulated by
other factors. For example, Ho (1978) altered both
light intensity and carbon dioxide concentration to
vary the photosynthetic rate of tomato leaves, but
found that the rate of export from those leaves was to
an appreciable degree independent of photosynthesis. We have similar results from barley (Table
4) : whilst leaves on plants grown at 700 ppm CO
#
photosynthesize and export faster than those on
plants at 350 ppm, just 24 h after a transfer between
CO concentrations the rate of export does not reflect
#
photosynthetic rate.
Source leaves would still dominate C flux if
sucrose export were a function of sucrose synthesis,
determined by the activity of sucrose phosphate
synthase (SPS). Activities of SPS correlate well with
rates of export (Huber, 1981), and SPS is allosterically regulated in a way that makes it a good
potential regulator. However the use of genetic
variants shows that SPS does not entirely regulate
export. Maize lines differing in SPS activity do not
demonstrate a simple relationship between SPS and
export (Rocher et al., 1994). Export is unaltered in
both transgenic tomato overexpressing SPS up to
sixfold (Galtier et al., 1995) and in potato underexpressing SPS (Geigenberger et al., 1995 ; FerrarioMery et al., 1997).
Another suite of hypotheses is based on the idea
that export is determined by sugar status. The
earliest such hypothesis suggested that the total
nonstructural carbohydrate content of the source leaf
drove export (Swanson & Christy, 1976 ; Ho &
Thornley, 1978), based on correlations between
sugar content and rate of export ; unfortunately the
slopes of the regressions between sugar and rate of
export were different in light and dark (Ho &
Thornley, 1978), suggesting that sugar status alone
is not a sufficient explanation. Export from barley
leaves is not simply predicted by total sugar status
(Table 4). It is probable that this sugar-mediated
export control hypothesis fails as it ignores compartmentation of sugars, both between and within cells.
Attempts to define just that pool of sucrose which is
readily available for transport, using compartmental
analysis (Farrar, 1989 ; Grantz & Farrar, 1999 ; B.
Collis et al., unpublished) find a hyperbolic relationship between export rate and the size of a pool of
sucrose which is readily transported (Farrar, 1999a).
There is no evidence that this relationship is
causal, and as barley mesophyll and parenchymatous
bundle sheath have differing carbohydrate contents
(Koroleva et al., 1998) it is necessary to seek further
information at the level of the single cell.
Last, it is possible that import by roots is regulated
by loading of phloem in source leaves. We do not
know if the number or activity of the transporters
which load sucrose into phloem (in plants which load
phloem apoplastically ; Buckhout & Tubbe, 1996 ;
Rentsch & Frommer, 1996) regulate phloem loading
and thus transport in vivo. Plants which are antisense
for a sucrose transporter do indeed export less
sucrose from source leaves (Riesmeier et al., 1994),
demonstrating the use of that particular transporter
but not that it has a role in control.
Evidence that regions outside the source leaf can alter
rate of import. Down-regulation of photosynthetic
capacity per unit of source leaf is direct evidence
against the hypothesis ; such evidence is now overwhelming (Moore et al., 1999 ; Stitt & Krapp, 1999)
and demonstrates that events outside the source leaf
partially determine the rate of carbohydrate production and thus its availability to roots. Photosynthesis describes C acquisition, but it does not
REVIEW
Control of carbon acquisition by roots
control it (Farrar, 1999b). Both the size and the
metabolic activity of sinks alter photosynthetic rate
and capacity (Marcelis, 1996).
Export itself is also partly dependent on sinks
remote from the source leaf (Moorby & Jarman,
1976 ; Geiger & Fondy, 1985). Lowering the temperature of the sinks can reduce export from source
leaves in both the short term (Minchin et al., 1994)
and the long term (Plum & Farrar, 1996). The
simplest interpretation of the data in Table 4 is that
when barley is transferred between CO concen#
trations, there is a residual effect of the CO
#
concentration at which the plants had been grown,
mediated via sinks downstream of the source leaf.
Overall, there is a considerable weight of evidence
against the view that import of C by roots is
regulated solely within source leaves, whether by
photosynthesis or by post-photosynthetic processes.
Hypothesis 3. Root carbon acquisition is controlled by
demand from within the root (‘ pull ’ hypothesis)
This hypothesis places the root in charge of its own
destiny : if there is a demand for C within the root,
this demand will simply be met by increased import
from the shoot. Implicitly, the shoot over-produces
carbohydrate and will never limit supply to the root,
and there have been suggestions to this effect
(Harper, 1977) although hard evidence is lacking.
The hypothesis is intuitively appealing because the
needs of the root for C are, by definition, met. If the
root is engaged in metabolically expensive uptake
and assimilation of nitrate, more C will flow to it ; if
growing rapidly in warm soil, sufficient C will flow to
it to support that growth.
What is root ‘ demand ’ ? Although the word ‘ demand ’
is frequent in the source–sink literature, it is rarely
defined, perhaps because it is hard to do so
meaningfully. There are three ways of defining
demand : (i) the current flux (the sum of fluxes
resulting in loss of C, which are listed in Tables 1
and 2, plus the C partitioned to growth) ; (ii) the flux
using the current machinery of enzymes and transporters but with no limitation from substrate ; and
(iii) the flux unconstrained by substrate supply when
the genes coding for all machinery have been
maximally induced. When demand is defined as the
flux when not limited by carbohydrate supply
(definitions (ii) and (iii)), hypothesis 3 is in any case
untrue.
The conventional components of demand –
growth, respiration and storage – are readily understood (Farrar & Williams, 1991). But those involving
loss of organic C compounds to the soil and to
symbionts need more consideration : are they driven
by events outside the plant, resulting in roots losing
C to the rhizosphere and its organisms at a rate
regulated by factors outside the plant?
47
Regulated carbon efflux. Exudation of C from roots
appears to be regulated under stress and seems to
achieve (i) the prevention of rhizotoxic chemicals
entering the root ; (ii) the removal of potentially
rhizotoxic chemicals from the root (C dumping) ;
and (iii) the enhanced mobilization and uptake of
nutrients under deficiency. Under these circumstances, C efflux from the root appears to be mediated
by anion channels which utilize the native electrochemical potential gradient across the plasma
membrane to gate the flow of organic acids into the
soil (Jones, 1998). For Al toxicity there is an anionspecific efflux channel which releases organic acids
only from the root apex in the presence of toxic levels
of Al (Ryan et al., 1995 ; Jones, 1998). The gating of
this channel appears to be directly regulated by
external Al concentration, is cell-specific and is
under the control of a single gene (Kochian, 1995).
Similar mechanisms have been proposed for lactate
efflux under anaerobiosis, and organic acid efflux
under P and Fe deficiency (Hoffland, 1992 ; Xia &
Saglio, 1992 ; Xia & Roberts, 1994).
Regulated carbon influx. The release of C compounds
into the rhizosphere causes a proliferation of microorganisms in the endo- and ectorhizospheres. While
some of these microorganisms improve plant fitness
(e.g. mycorrhizas, N -fixing bacteria), the rhizo#
sphere is also a primary point of pathogen entry.
There is little competitive advantage in the loss of
simple sugars and proteinaceous amino acids to the
rhizosphere, as they have little nutrient complexing
power and rarely act as specific microbial signals
(Jones et al., 1994). The plant reduces the net C loss
by active uptake of these low molecular weight
compounds from the soil via H+–ATPase-driven
proton cotransporters (Fig. 1). These transporters
are typically constitutively expressed in all regions of
the root and appear to be capable of recapturing
large amounts of lost C under hydroponic and soil
conditions (Jones & Darrah, 1994, 1996). Although
the competitive influence of the soil microbial
biomass on this C retrieval mechanism has yet to be
quantified, based on independent kinetic studies
(Km, Vmax) it appears that competition will be strong
(Jones & Hodge, 1999). In addition to recovery of its
own C, this C retrieval mechanism may also
significantly contribute to N uptake (Chapin et al.,
1993).
As influx and efflux of C compounds from the root
are both at least partly root-regulated, this component of root demand is set by the root itself but in
response to conditions in the rhizosphere, so the
latter has a role in determining C fluxes in roots.
Do plants overproduce carbohydrate? The hypothesis
is disproved if plants do not overproduce carbohydrate. Well, do they? We argue that they do not.
The pools of carbohydrate which seem large, say
48
REVIEW
J. F. Farrar and D. L. Jones
Table 5. Respiration in leaves and roots of barley in
extended darkness
Parameter
Leaf
Days in dark
Rate of respiration
CHO content
Protein content
2
58
11
61
Root
4
—
5
23
8
—
9
5
2
100
53
67
4
92
53
72
8
46
65
32
Values are percentage value before darkening. At the time
of darkening, roots contain enough carbohydrate to sustain
respiration for 6 h at control rates. Unpublished data of P.
Dwivedi & J. F. Farrar.
10% of plant dry weight, are in fact small compared
to the fluxes through them. A plant growing at 0.25
d-" is turning over these pools rapidly, and the pools
of soluble carbohydrate in cytosol of leaf and root
have half-times of less than 2 h (Farrar, 1999a).
Further, there are mechanisms to prevent overproduction of sugars, notably the down-regulation of
photosynthetic machinery when sugars accumulate
(Farrar et al., 2000). It seems that the size of pools of
sugar which are rapidly turned over can increase
quickly when supply exceeds demand, and begin to
down-regulate the machinery which produces the
sugars.
Is import into the root determined by root demand?
When plants are kept in the dark for prolonged
periods, the relative response of shoot and root is
remarkable. In the potentially vulnerable root tissue,
with low contents of nonstructural carbohydrate,
root respiration and growth rate decline only after
several days during which sugar, starch and protein
contents, and activities of key respiratory enzymes,
are little affected (Table 5 ; Farrar, 1999a), although
the initial content of carbohydrate in these roots is
sufficient to sustain metabolism for only a few hours
at the control rate. Roots lose metabolic capacity
only after darkening for 6 d. Source leaves are quite
different : carbohydrate content (initially very high),
protein content and respiration rate all fall within
1–2 d of darkening, and there is loss of photosynthetic and respiratory enzymes. The unexpected
reason is that the shoot continues to export carbohydrate to the root for many days, so root metabolism
is supported. Surprisingly, it is the shoot, far richer
than the root in carbohydrate when the plant is first
darkened, which first shows the effects of darkening.
This is a striking example of root demand having a
large effect on import. Other examples were given
when discussing the ‘ push ’ hypothesis.
However, there is also evidence against the ‘ pull ’
hypothesis. If photosynthesis is increased, by supplying either more light or increased concentrations
of CO , roots import more C and grow more quickly
#
(Table 3). Do sinks usually grow at less than their
maximum possible rate? A series of experiments on
barley roots (Bingham & Farrar, 1988 ; Farrar &
Williams, 1991) showed that growth and respiration
rate of the roots on fast-growing, intact plants could
be increased by treatments which caused a sustained
increase in assimilate inflow to the root. A similar
conclusion comes from experiments on increased
atmospheric CO (Collis et al., 1996 ; Farrar, 1999a).
#
In these and other experiments, the data are
consistent with the following. When the supply of
sugar is greater than demand of a root, respiration
and metabolism do rise, but only after a lag consistent
with inducing coarse control. The amount of transcript for a range of enzymes rises (Farrar, 1999a ;
Koch, 1996, 1997 ; B. E. Collis et al., unpublished),
in a manner consistent with sugar supply being a
signal regulating gene expression (Farrar et al.,
2000).
Mechanism by which root demand might be signalled to
the phloem. An integral part of a hypothesis based on
root ‘ pull ’ is that metabolic events in receiver cells in
the root must be transmitted to the phloem in which
import takes place. We have no idea what the
mechanism might be. Patrick & Offler (1995) have
pointed out that it cannot be the low carbohydrate
status of bulk tissue which directly stimulates
import, as the concentrations of sugars in roots are
too low to alter appreciably the turgor of phloem
within the tissue (and Table 3 shows that barley
roots growing fast due to elevated atmospheric CO
#
have high sugar contents). It might be a combination
of turgor in expanding cells (Farrar et al., 1994 ;
Pritchard, 1998) and gating of the plasmodesmata
which connect them to the phloem (A. Schultz,
pers. comm.). Although plasmodesmatal gating is
still not fully understood, turgor in expanding cells
will be in part a consequence of the rate of use of
assimilate and ions versus their rate of import, and
thus could act as a direct mediator of metabolic
activity in the key region of the growing root.
Relationships with the activity of acid invertase
might be correlations rather than causal ; certainly
there is no satisfactory complete explanation centred
on invertase.
Overall the evidence supporting the ‘ pull ’ hypothesis is more than balanced by evidence which
disproves it. However, there is clearly sense in the
demand from roots having some role in regulating
import from the shoot, just as there is sense in
availability of assimilate in sources having a role in
how much goes to roots. Can these two, apparently
opposite, hypotheses be reconciled?
Hypothesis 4. The control of acquisition of carbon by
roots is distributed around the plant in shoot and root
(‘ shared control ’)
If neither ‘ push ’ nor ‘ pull ’ hypothesis is completely
successful, yet each fits some of the evidence, it
REVIEW
Control of carbon acquisition by roots
Table 6. Top-down metabolic control analysis of
carbon flux in single-rooted soybean leaves
Age of single-rooted
leaves (d)
Parameter
14
16
Leaf\root d. wt
Control in source leaf
Control in root
2n02
0n64
0n36
1n42
0n79
0n21
Control coefficients are given for a two-block system
where the source leaf produces and the root consumes the
common intermediate sucrose. Unpublished data of S.
Gunn & J. F. Farrar.
seems that each of these hypotheses is too simple.
Rather, it might be that control of root C acquisition
resides partly in the root and partly in the shoot.
Such a suggestion may appear less elegant than
either the ‘ push ’ or the ‘ pull ’ hypothesis, yet it
seems intuitively reasonable that both the availability
of, and the need for, assimilate are involved in
determining its flux to roots. Here we examine the
general hypothesis that control of import into roots
is shared between shoot and root.
There is both a theoretical argument, and evidence, to support the idea of distributed control.
These have been described in the context of leaf
properties being determined partly from outside the
leaf (Gunn et al., 1999b) ; for sinks in general
(Farrar, 1996) and for whole plants (Farrar, 1999b).
The theory is that of metabolic control analysis (Fell,
1997). Its central tenet is that in complex, multistep
linear or branched systems, every step contributes to
the control of flux and so control is distributed
throughout the system. Some steps could contribute
much more control than others, but all contribute.
In a linear system, the control coefficients which
define the control at each step sum to 1. The task of
metabolic control analysis is to measure experimentally just how much control is associated with
each step of a pathway ; transgenic plants, particularly those over or underexpressing an enzyme of
interest, have become favoured tools for such
investigations (Stitt, 1996).
There are two approaches to applying top-down
metabolic control analysis to whole plants. Sweetlove
et al. (1998), using transgenic potato and "%C to
49
estimate flux, conclude that about 80% of control
resides in source leaves and the remainder within
sinks. We have adopted a single-source : single-sink
system, rooting a soybean leaf from the base of the
lamina, to obtain a single source of unchanging
photosynthetic area supplying assimilate to a single
sink – a root system growing at a constant absolute
rate. The merit of this system is that sucrose
produced in the source lamina has only two significant fates : storage in the lamina, or export to the
root. No other sinks are available to it ; thus a major
handicap of working on normal plants with their
multiple sources and sinks is eliminated. A potato
plant with an antisensed gene expressed in its tubers
still has fibrous roots and meristems in the shoot as
alternative sinks for assimilate from source leaves,
for example. Our initial data (Table 6) ascribe c.
80% of control of C flux to the source leaf, and c.
20% to the root. (We would argue that our agreement
with the data of Sweetlove et al. (1998) is fortuitous
rather than fundamental.) We have also used a
method analogous to, but simpler than, metabolic
control analysis (Farrar & Gunn, 1998), calculating
response coefficients sensu Jones & Lynn (1994) for
plants which have been partially defoliated. The
argument is that if whole-plant growth is controlled
solely by the photosynthetic acquisition of C, then a
reduction of (say) 40% in photosynthesis should be
matched by a 40% reduction in growth. The
proportionality is calculated as a response coefficient.
For two different species, we have shown that growth
is reduced less than would be expected when we
remove a significant proportion of the leaf area, and
the reduction of growth is less at 700 than at 350 ppm
CO (Table 7). Our interpretation is that before leaf
#
area was removed, the growth of these plants was
partially limited by their sinks, c. 40% of which
are roots, and that limitation by sinks was greater at
700 than at 350 ppm CO . Control of growth is thus
#
shared between source leaves and sinks.
Additional evidence for shared control of growth. With
the benefit of hindsight, it is possible to use existing
literature and commonplace observations to support
the idea of shared control of C flux. First, the
transport system probably has a role in control, as
the length of the transport pathway affects flux to
sinks (Canny, 1973 ; Cook & Evans, 1978 ; Minchin
Table 7. Response coefficients for two species grown at two concentrations of CO
#
Species
Parameter
Dactylis glomerata
Bellis perennis
CO concentration (ppm)
#
Response coefficient
350
0n85
350
0n98
700
0n03
700
0n56
Plants were partially defoliated 2 d before harvest and response coefficients calculated as the ratio between proportional
reduction in subsequent growth and proportion of leaf area removed.
50
REVIEW
J. F. Farrar and D. L. Jones
et al., 1993) and short-distance transport within
sinks may present further constraints (Bret-Harte &
Silk, 1994 ; Patrick & Offler, 1995). Models of
phloem transport also show clearly that there is the
potential for control by transport itself (Minchin et
al., 1993).
Many of the experiments which have been explicitly designed to address the problem of whether
growth is limited by sources or by sinks are
unsatisfactory. If control is indeed distributed around
the plant, an experiment designed qualitatively to
detect the presence of some source limitation should
find it ; but so should an experiment designed to test
for sink limitation. The literature is therefore littered
with opposing qualitative claims about whether
source or sink limits growth. They can all be
reconciled with a view that control is distributed
around the plant and indeed includes control by
fluxes between plant and both rhizosphere and
symbionts. Some of these experiments have been
mentioned in discussing the ‘ push ’ and ‘ pull ’
hypotheses.
It is also possible to explain the effects of the
environment on plants if control of growth is
distributed. For example, the growth of one variety
of Dactylis glomerata under a fixed set of conditions
can be increased either by increasing the ambient
CO concentration, or by raising the temperature
#
(Farrar, 1999b). Such an effect is commonplace. We
interpret this observation as co-limitation of wholeplant C flux by photosynthesis (CO increases
#
growth because photosynthesis is CO -limited) and
#
sink growth (temperature increases growth because
metabolism within sinks, and in particular cell
division, is highly temperature-sensitive whereas
photosynthesis is not). Both source and sink must
have been limiting growth together before the
treatments were applied. We argued above that
conditions in the rhizosphere affect root C flux : is
the converse true? Can an increased supply of
carbohydrate to the root increase exudation? Shortterm experiments on plants exposed to increased
atmospheric CO concentrations suggest not (S.
#
Plum and J.F. Farrar, unpublished), although there
are claims to the contrary. Increasing photon flux
density certainly does not (Hodge et al., 1997). (For
both light and CO it is necessary to distinguish
#
carefully between the amount of root, increased by
higher C flux, and exudation per unit of root,
unaltered by C flux.)
Mechanisms underlying shared control of carbon flux.
So far we have demonstrated that control of C flux is
distributed, and a means of quantifying that distribution. It remains to show that there are
mechanisms consistent with the hypothesis. We
propose that phloem transport, together with gene
regulation by sugars and other resource compounds,
provide sufficient mechanism.
The mechanism by which phloem operates is
believed to be pressure flow, driven by gradients of
turgor pressure between source and sink. The
consequence of phloem operating by pressure flow is
that neither machinery for sucrose production, nor
the amount of sugar in the leaf in any pool, would be
expected to determine the rate of export. Rather, the
rate must be a function of several factors in source
leaf, phloem conduits and in sink which jointly
determine turgor gradients in the phloem and
solution flux in response to those gradients. Import
into roots becomes a whole-plant property (Farrar,
1992, 1996 ; Minchin et al., 1993). Indeed, once
there is more than one source or sink the system
behaves in a complex way which is not intuitively
obvious. For example, when one source is supplying
two dissimilar sinks, the proportioning of assimilate
between the two sinks changes with the flux out of
the source. There need not be any simple link
between the turgor established in the phloem (which
will determine solvent flux in the phloem) and
metabolism in the tissue containing it ; nor need
there be a simple link between sugar loaded into the
phloem and turgor generation, as many other solutes
contribute to turgor.
The second mechanism is the regulation of gene
expression by resource compounds, particularly
sugars and compounds of nitrogen. Details of this
idea are discussed by Koch (1996) and Farrar et al.
(2000). In essence, the expression of genes encoding
proteins key to source leaf and sink metabolism is
regulated by sugars, nitrate or amino acids.
Typically, photosynthetic genes are down-regulated
and sink metabolism genes up-regulated by high
sugar concentrations. The idea is appealing because
of its neatness and its symmetry : plentiful carbohydrate regulates whole-plant metabolism both to
reduce its production and to increase its consumption ; a shortage does the reverse (Koch, 1997). As
the signal molecules, or their close metabolites, are
xylem or phloem mobile, they can take messages of
sugar and N status from leaf to root and vice versa.
Clearly such a system means that control of C flux is
shared, as, for example, the capacity of a root to
metabolize sucrose (and thus sustain its import) will
be set by the history of sugar supply from the shoot
(Table 3 ; Bingham & Farrar, 1988 ; Farrar et al.,
2000). The rapid turnover of pools of total nonstructural carbohydrates such as sucrose means that
a small change in flux can result in a large change in
pool size. The sugar status of a tissue thus is a timeintegrated sensor of the balance between production
and consumption of sugars under varying environmental conditions. There is an urgent need to test
the broad hypothesis that resource compounds
regulate the expression of key genes in real plants in
real situations : too much of the evidence supporting
this idea comes from artificial laboratory systems for
us yet to feel sure of its importance.
REVIEW
Control of carbon acquisition by roots

We conclude that there is qualitative and quantitative
evidence supporting the hypothesis that control of C
flux into roots is shared between the many processes
which contribute to whole-plant C flux, including
those determining loss of C from the root to soil and
its organisms. For those wanting a crude approximation of the flux to root growth, a percentage of
photosynthesis characteristic of that species and its
rooting and aerial environment may suffice. Better
approximation needs good mechanistic modelling,
and we are not aware that an adequate model exists.
We emphasize that the shared control hypothesis is
not a restatement of functional equilibrium, although
the underlying mechanisms could explain the
phenomena described by the functional equilibrium
hypothesis.
Finally it remains to speculate on the consequences
for climate change impacts : what would CO and
#
temperature be expected to do? Some of the issues
have been discussed before (Farrar & Gunn, 1996 ;
Gunn et al., 1999a ; Farrar, 1999a). The implications
of our argument for rising CO are : to a first
#
approximation, plants will simply be bigger, with
bigger root systems as a consequence of their size but
with little or no change in C partitioning to them
(Table 3). However, as these large plants have more
demand for nutrients and water, and the soil is
relatively depleted in these resources as a consequence, there will be more growth of root relative to
shoot directed by mechanisms as yet unknown, and
if soil nutrients are low there might also be more
exudation from roots and C transfer to mycorrhizas
(Fitter et al., 2000 ; Treseder & Allen, 2000) ; but
these effects of elevated CO will be indirect.
#
We also urge that for many future experiments it
might be helpful to identify where most control is
localized, as this is where external or genetic
manipulation will be most effective. This will soon
be a possibility for whole plants grown hydroponically, but its application to plants in ecosystems
is further away.
              
We would like to acknowledge the financial support of the
BBSRC, the NERC and DFID.

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