Download Vascular Architecture of a Large-leafed Genotype of Trifolium repens

Annals of Botany 81 : 441–448, 1998
Vascular Architecture of a Large-leafed Genotype of Trifolium repens
N. R. S A C K V I L L E H A M I L T O N*† and M. J. M. H A Y‡
* EnŠironmental Biology Department, Institute of Grassland and EnŠironmental Research, Plas Gogerddan,
Aberystwyth, Ceredigion SY23 3EB, UK and ‡ Grasslands Research Centre, AgResearch, PriŠate Bag 11008,
Palmerston North, New Zealand
Received : 21 October 1996
Returned for revision : 10 February 1997
Accepted : 24 November 1997
The objectives of this study were to identify the vascular connections from roots to upper axial bundles in one
genotype of Trifolium repens L. ‘ Grasslands Kopu ’, identify pathways followed by the transpiration stream, and
establish whether these pathways could account for previously-observed patterns of clonal integration. The study
provides new information on vascular connections between root and parent and branch stolons at nodes possessing
both a root and a branch, and to the first two leaves on branch stolons. A nodal root is connected to the lower nearside
axial bundle of the parent stolon but to both lower and upper nearside axial bundles of the branch. Upper sympodia
provide a long-distance transport pathway from a parent stolon to the apex of branch stolons. Lower sympodia are
functionally different, providing short-distance transport to structures in close proximity to the source root. This is
consistent with observed patterns of clonal integration in T. repens and may provide a simple architectural mechanism
facilitating foraging.
# 1998 Annals of Botany Company
Key words : Acid fuchsin, clonal integration, foraging, physiological integration, serial sections, white clover,
Trifolium repens (L.), vascular architecture, xylem transport.
I N T R O D U C T I ON
The architecture of the vascular system of a plant is one of
the major determinants of patterns of resource allocation
and, therefore, of clonal integration between connected
parts of the plant (Watson and Casper, 1984 ; Price, Marshall
and Hutchings, 1992). Patterns of clonal integration, in
turn, determine the potential of the plant to ‘ forage ’
(foraging : ‘ the processes whereby an organism searches, or
ramifies within its habitat, which enhance its acquisition of
essential resources ’ ; Hutchings and de Kroon, 1994). A
knowledge of vascular architecture is, therefore, a prerequisite for studies on clonal integration and foraging.
The growth habit and dynamics of Trifolium repens—a
long-lived perennial herb often present as mobile patches in
heterogeneous grasslands, and persisting by the indefinitelyrepeated production of short-lived nodes on laterallyspreading shoots (often now described as stolons)—suggests
an important role for foraging. Yet studies on clonal
integration and foraging in this species are constrained by
inadequate knowledge of its vascular architecture. In
particular, published descriptions of the vascular architecture of T. repens (Erith, 1924 ; Devadas and Beck, 1972 ;
Thomas, 1987 ; Fig. 1) contain an anomaly. The vascular
system is reported to comprise eight to nine or more
vascular bundles in four sympodia. Each sympodium
consists of one axial bundle and associated leaf traces,
branch traces and other bundles that branch repeatedly
from the axial bundle in a regular sequence. Each axial
bundle is continuous from base to apex of a stolon. There
† For correspondence. Fax 01970 828357, e-mail Ruaraidh.
Hamilton!BBSRC.AC.UK
0305-7364}98}030441­08 $25.00}0
are no connections between the two upper and two lower
sympodia. Nodal roots (the literature does not indicate
whether derived from upper or lower root primordia) are
connected only to the axial bundles of the lower sympodia.
Essentially the same architecture was confirmed by
A. Bryan, N. R. Sackville Hamilton and A. D. Bell (pers.
comm.) in stolons from a wild population of T. repens in
North Wales. The anomaly is that there appear to be no
vascular connections from roots to upper sympodia, i.e. no
pathway enabling the latter to perform their function of
carrying the transpiration stream from root to leaf. One
objective of the work reported here was to identify such
pathway(s) so as to provide the necessary basic information
for studies on clonal integration and foraging.
The clonal integration expressed by T. repens shows an
unexplained and unpredicted complexity (Turkington,
Sackville Hamilton and Gliddon, 1991). On the one hand,
stolon apices are highly integrated. When branches on the
two sides of a stolon were grown with different species of
grass, apices of the branches on both sides differentiated
new modules (¯ node­leaf­proximal internode­axillary
bud­nodal root) at the same rate, although the common
rate was different under different pairs of grasses. It was
suggested that this enables exploratory lateral spread of the
plant to continue through locally-unfavourable as well as
favourable patches : clonal integration is essential to support
this component of growth when resources are not abundant
locally.
On the other hand, differentiated modules showed a
localized, unintegrated response, changing leaf area and
development of axillary buds in response to their immediate
microenvironment but being unaffected by the micro-
bo970576
# 1998 Annals of Botany Company
442
SackŠille Hamilton and Hay—Vascular Architecture of Trifolium repens
transpiration stream of the upper two sympodia, and that
transport within the two lower sympodia is primarily shortdistance. It is proposed that, if the hypothesis is confirmed,
it would provide a mechanism for the simultaneous high
clonal integration of lateral spread, and localized,
unintegrated responses of modules to favourable patches.
MATERIALS AND METHODS
F. 1. Vascular system of a stolon of Trifolium repens as published by
Thomas (1987). Bud traces (O) are shown as broken lines, and vascular
connections of nodal roots (RT) as dotted lines. M, L, and U are
median, lower and upper leaf traces, respectively. Axial bundles are
labelled A1 to A4, in accordance with the nomenclature of Thomas
(1987). Reproduced by kind permission of the Commonwealth
Agricultural Bureau, with node numbers and trace labels altered to
conform with the conventions adopted here.
environment of connected branches on the opposite side of
the stolon. It was suggested that increasing leaf area and
branch production enhances exploitation of favourable
patches once they are encountered, and that localized,
unintegrated responses of these characteristics ensure that
exploitatory growth responses are restricted to favourable
patches.
Implicit in this finding is that control of resource allocation
to apical meristems must be fundamentally different from
that to the differentiated products of meristems. Resource
allocation to apical meristems should be possible over long
distances within the plant, whereas other sinks should
receive resources primarily from local sources.
This paper reports on experiments designed to test the
hypothesis that vascular connections from roots to upper
sympodia enable long-distance transport to occur within the
Sixty cuttings of a genotype of the large-leafed variety
‘ Grasslands Kopu ’, AgResearch clone K131, were established in potting compost in seed trays in a glasshouse in
Palmerston North, New Zealand during January (summer).
After 8 weeks, patterns of transport in the xylem were traced
with acid fuchsin using a methodology based on Roach
(1939) and Price et al. (1992). At this stage, the plants had
16–18 nodes on the parent stolon, with each mature node
bearing either an inflorescence or a branch. Forty plants
were selected and treated in the following manner. A single
nodal root attached to each plant was teased out of the
compost and washed. A 1±5 cm$ vial containing a 0±5 %
aqueous solution of acid fuchsin was embedded in the soil
below the relevant node, the root was inserted and then
severed, under the solution, at 2 cm below the node. All
other roots of the plant remained in place in moist potting
compost during the period of uptake of dye. After 3 to 10 h,
the distribution of dye was noted where visible on the intact
plant. Transverse sections through fresh stolons of labelled
plants were taken just proximal (i.e. towards the base of the
stolon) to each node and drawn to show which vascular
bundles contained dye. Serial sections were cut through
selected nodes and internodes after labelling.
Forty plants were treated thus, supplying one root on
each plant with acid fuchsin. To determine transport
patterns over the whole plant, a range of positions was
selected for the treated root, from the youngest to the oldest
rooted node on a stolon (Table 1, control), and on the first
five nodes of a branch stolon (Table 1, branch). The path
followed by the transpiration stream depends on the
distribution of sources (roots) and sinks (leaves and other
evaporative surfaces). These were controlled in some plants
by selecting plants with particular characteristics (Table 1,
unrooted), by removing selected branches, roots and}or
leaves, or by severing selected stolon internodes, 24 h prior
to labelling (Table 1, cut and severed treatments).
Directions ‘ left ’ and ‘ right ’ are given viewing a stolon
from above its base towards its apex. Nodes are numbered
acropetally starting with the treated node as node 0 ;
negative node numbers indicate nodes proximal to the
treated node. There appears to be no accepted terminology
corresponding to ‘ adaxial ’ and ‘ abaxial ’ to describe the side
of a parent stolon relative to the side bearing a branch. For
both parent and branch stolon the term ‘ nearside ’ is used to
refer to the same side as the axil and ‘ farside ’ to refer to the
opposite side, noting that for the branch, but not for the
parent, ‘ nearside ’ is the same as ‘ adaxial ’ and ‘ farside ’ the
same as ‘ abaxial ’.
SackŠille Hamilton and Hay—Vascular Architecture of Trifolium repens
T     1. Summary of positions of roots of Trifolium repens
supplied with acid fuchsin, and of treatments applied
Treatment
(replicates)
Control (25)
Cut branch 0
(2)
Unrooted
distally (2)
Cut distal (2)
Severed
stolon
proximally
(2)
Supply acid
fuchsin to
branch (5)
Supply acid
fuchsin to
branch, cut
stolon
proximally
(2)
Objective}hypothesis
Supply acid fuchsin to the
root at one branched
node on a profuselybranched plant. Node
position ranging from 4
to 15 nodes from the
apex, the branch having
1–3 nodes less than the
number of distal nodes
on the parent
As control, but node
position 7–8 nodes from
apex, and branch at node
0 removed 24 h prior to
application of acid
fuchsin
As control, but node
position 7–8 nodes from
apex, on stolons with no
roots distal to the treated
root
As control, but node
position 7–8 nodes from
apex, and all
inflorescences, branches,
roots, and leaves distal to
the treated root removed
24 h prior to treatment
As control, but node
position 7–8 nodes from
apex, and severed parent
stolon at the second
internode proximal to the
treated root
Treated root is on branch,
1–5 nodes from the point
of insertion of the branch
into its parent stolon.
Branch position 6–9
nodes from apex of
parent
As previous treatment, but
treated root 1–2 nodes
from branch’s point of
insertion into its parent
stolon, and severed the
parent stolon at the
second internode
proximal to the origin of
the treated branch.
Standard transport
patterns in a plant
growing under
optimal conditions
Improve sensitivity of
analysis of transport
paths into branch at
node 2 by increasing
transport into that
branch
Presence of distal
roots (sources) may
affect transport
patterns
Presence of distal
sources and sinks
may affect transport
patterns
Presence of proximal
sources may affect
transport patterns
Basipetal transport
from branch to
parent
Presence of proximal
sources may affect
basipetal transport
from branch to
parent
443
Superficial distribution
Dye in leaves and stipules was visible without dissection
(Fig. 2). Dye in stolons and petioles was not visible
superficially. The distribution of dye was apparent after 2 h
and intensified, with no qualitative changes, during a 10 h
period.
Regardless of which root was treated, acid fuchsin entering
any leaf through its median leaf trace dyed the terminal
leaflet and the distal two thirds of both lateral leaflets
heavily (Fig. 2 A). Dye entering through upper and lower
leaf traces stained the uppermost and lowermost half of the
leaf, respectively, i.e. lateral leaflet plus half of the terminal
leaflet (Fig. 2 A). (The left side of a leaf is uppermost in
leaves originating on the left side of the stolon, and the right
uppermost in leaves on the right.) The regions of leaf
supplied by the upper trace do not overlap with those
supplied by the lower. The intensity of staining was greatest
in that part of the lateral leaflet not also supplied by the
median trace but, even there, the intensity was lower than in
leaves receiving dye through the median trace. In addition,
dye in the upper leaf trace stained the upper stipule (Fig.
2 B).
Transport paths from root to shoot
The vascular system of the root divides into two unequal
bundles to form separate direct connections to the vascular
systems of both parent and branch (Fig. 3). The smaller root
bundle connects to one bundle—the lower nearside axial
bundle—of the parent, while the larger root bundle spreads
out to connect directly to several nearside branch bundles,
including both lower and upper nearside axial bundles.
In accordance with these connections, dye absorbed by
the root at a branched node entered both parent and branch
stolon at that node. The parent stolon received dye only in
the lower nearside axial bundle. The branch stolon at that
node received dye in at least three vascular bundles : the
lower and upper nearside axial bundles and the median
trace to the leaf at the first node on the branch. Up to three
further bundles in the branch received smaller amounts of
dye in some plants, all on the nearside of the branch.
Conforming with the sizes of the two root bundles, and
the number of vascular bundles carrying dye in the stolon,
most dye entered the branch at node 0 rather than the
parent stolon, especially in well-developed branches.
Transport paths within a parent stolon
RESULTS
As in most field- and glasshouse-grown plants of Trifolium
repens, roots developed only at the lower of the two root
buds at each node. Thus no data can be presented on
transport from roots developing from the upper bud.
Much or all of the dye entering the parent stolon was
transported into the leaf at node 2 through its median leaf
trace, the nearest available sink (Fig. 1). No dye appeared in
the leaf at node 0, in accordance with the absence of
vascular connections between the root and leaf of a node
(Fig. 1). The presence of a developing inflorescence or
branch at node 2 often caused acropetal transport in the
lower and}or upper axial bundle as far as that branch or
inflorescence.
Further transport along axial bundles could be induced
444
SackŠille Hamilton and Hay—Vascular Architecture of Trifolium repens
F. 2. Superficial appearance of Trifolium repens labelled with acid fuchsin in (A) leaves receiving acid fuchsin through (right) the median or (left)
a lateral trace supplying the right side. B, Upper stipules with (bottom) or without (top) acid fuchsin in the upper leaf trace.
by manipulation (Table 2). Removal of the leaf and branch
at the treated node and of all distal leaves, branches and
inflorescences caused dye to be transported the full length of
the stolon in both upper and lower nearside axial bundles.
The absence of roots distal to the treated root had no effect
on dye transport along the upper axial bundles (i.e. there
was no transport with or without distal roots), but increased
transport in the lower sympodium such that dye moved up
to four nodes distally in the axial bundle to supply the
median leaf traces at nodes 4 and 6.
Serial sections through the internode distal to a root
showed that a vascular bundle branches from the lower
nearside axial bundle, i.e. the one supplied by the root, and
anastomoses with the upper nearside axial bundle. In some
plants, dye passed up this bundle and appeared in the upper
nearside axial bundle at node 1. In other plants, dye
remained in the lower nearside axial bundle at node 1.
In no case did dye cross from left to right axial bundle or
Šice Šersa across a stolon. However, if dye was present in
one upper sympodium then in some cases it appeared in the
upper traces of leaves on both sides without crossing to the
other upper axial bundle.
SackŠille Hamilton and Hay—Vascular Architecture of Trifolium repens
445
T     2. Summary of effects of treatment on transport of
acid fuchsin in Trifolium repens
Treatment
Effect
Cut off branch at
node 0
Caused consistent heavy transport into
branch at node 2, via upper and}or lower
axial bundles
Increased the distance of acropetal
transport in lower axial bundles by up to
4 nodes. No effect on acropetal flow in
upper axial bundles
Caused acropetal transport along the full
length of the stolon to the apex in both
lower and upper axial bundles
Distal nodes unrooted
F. 3. Topological 3-D diagram of vascular connections between root
and axial bundles at a node of a stolon of Trifolium repens with a root
and a branch to the right. The diagram includes one proximal internode
on the parent stolon to show the point of insertion of the upper branch
trace at the proximal node. For simplicity, leaf traces and other
connections are not shown, and topographical features, such as the size
and shape and positions of the bundles within the stolon, are not
depicted accurately. Unshaded bundles, four axial bundles of the
parent stolon, oriented with the base of the stolon towards the top left
and its apex towards the bottom right ; lightly shaded bundles, four
axial bundles of the branch stolon and branch traces within the parent
stolon ; heavily shaded bundles, vascular bundle from the root and its
connections to axial bundles in the stolons. Axial bundles in the parent
stolon are labelled A1 to A4 following the convention of Thomas
(1987), and A1« to A4« in the branch stolon.
Basipetal transport was induced by severing vascular
connections to organs usually supplied from proximal
roots. For example, severing the root at node ®2 and the
stolon internode proximal to node ®2 in a stolon caused
basipetal transport along the axial bundle to supply the
median trace of leaf 0 (Table 2).
The qualitative patterns of distribution of dye within the
parent stolon from a treated root were not affected by the
position of the root along the stolon. Sections through
nodes and internodes confirmed that the vascular connections shown in Fig. 1 correctly describe all nodes along
the full length of a stolon. As nodes age, there is secondary
thickening of the vascular bundles but no changes in the
vascular connections.
Transport into branch stolons
Both lower axial bundles in the branch (A1« and A4« in
Fig. 3) are derived from the lower nearside axial bundle in
the parent (A4). Both upper axial bundles in the branch
(A2« and A3«) are derived from the upper nearside axial
bundle in the parent (A3) via a branch trace extending one
node proximally within the parent stolon.
In accordance with these and the previously-described
root-shoot connections, dye from a treated root did not
appear in branches on the farside of the parent stolon
Cut off inflorescences,
branches, roots, and
leaves at all distal
nodes
Cut through parent
stolon at second
internode proximal
to the treated root
Supplied acid fuchsin
to root on branch,
1–5 nodes from base
of branch
Supplied root on
branch, 1–2 nodes
from base of branch ;
parent stolon severed
at second internode
proximal to parent
node of treated
branch
Caused transport into the leaf at node 0 via
its median trace, by basipetal transport in
the lower nearside axial bundle to the
point of insertion of the trace
Qualitatively similar to control
Marked basipetal transport from second
branch node into parent stolon, thence
into median trace of leaf at treated node.
Little basipetal transport from first branch
node
(nodes ®1, 1, 3, 5 etc.). Basipetal transport within the parent
stolon was not sufficient in any plant for dye to appear in
nearside branches proximal to the treated root (nodes ®2,
®4 etc.). Dye appeared predominantly in the branch at node
0 but also in distal nearside branches (nodes 2, 4 etc.).
Dye entering a branch in an upper axial bundle was
transported the full length of the branch, in branches of any
size from three to 14 nodes. Dye entering the branch in a
lower axial bundle was transported two to three nodes if
branch nodes themselves were rooted, or four to five nodes
if the branch nodes were unrooted.
Vascular bundles in a branch stolon diverged from
bundles in the parent stolon proximally to the point of
insertion of the root at the same node (Figs 3 and 4). Dye
passed directly from the root into the branch at node 0, but
distal nearside branches received dye only via bundles in the
parent stolon. Therefore the pattern of distribution of dye in
the branch at node 0 was qualitatively different from that
observed in distal nearside branches.
Transport within the branch at node 0
The branch at node 0 received dye in its nearside bundles
only (the only bundles that are connected to the root of the
parent node). The first leaf was dyed through its median
trace, which has a strongly-developed connection to the
root at node 0, and was consistently the most heavily dyed
of all leaves on the plant (Fig. 4 A). The appearance of dye
in subsequent leaves of the same branch was in accordance
446
SackŠille Hamilton and Hay—Vascular Architecture of Trifolium repens
L2
*
F. 4. Vascular connections from a parent stolon to the first four leaves of a branch stolon of Trifolium repens. For clarity, separate diagrams
are presented for (A) lower and (B) upper sympodia. Connections with roots and secondary branches arising from the branch stolon are not
shown. Thick lines, leaf traces ; thin lines, axial bundles ; solid lines, bundles in branch ; dotted lines, bundles from root ; dashed lines, connecting
bundle in parent stolon, i.e. lower nearside axial bundle for lower sympodia (A), branch trace for upper sympodia (B). Nodes are numbered from
the base of the branch, and lower, median and upper leaf traces to node n (n ¯ 1 … 4) are labelled Ln, Mn, Un. Asterisks indicate bundles receiving
dye when dye is supplied to the root of the parent node : ***, consistently and heavily stained ; **, consistently stained ; *, stained, but lightly or
not consistently.
with previously-published vascular connections (Fig. 1),
given the new finding that only the nearside vascular
bundles have vascular connections from the root at node 0
(Figs 3 and 4). The second leaf was dyed, lightly or not at
all, through its lower trace, and the third was consistently
dyed through its median trace (Fig. 4 A). The fourth leaf
was consistently dyed through its upper trace (Fig. 4 B), and
was the most proximal leaf on the branch to be thus dyed.
Appearance of dye in subsequent leaves and stipules was
more variable.
Transport within distal nearside branches
Distal nearside branches received dye in their farside as
well as their nearside bundles. Dye appeared only in the
lower bundles, or only in the upper ones, or in all bundles,
depending on whether it entered from the lower or upper or
both nearside axial bundles of the parent stolon (Fig. 3) (the
occurrence of these three possibilities is described above).
Leaves in these distal branches were dyed through their
traces in accordance with the connections shown in Fig. 4,
i.e. through traces shown in Fig. 4 A if the branch received
dye via the lower nearside axial bundle of the parent stolon,
and those shown in Fig. 4 B if it received dye via the upper
nearside axial bundle of the parent. The most proximal
leaves were the most heavily dyed, and median traces
carried more dye than lateral traces.
Basipetal transport
Marked basipetal transport from branch to parent stolon
was observed when the root of the second node on a branch
was treated and the parent stolon was severed at the
internode two nodes proximal to the node at which the
branch originated (Table 2). In contrast, little or no basipetal
transport into the parent occurred when the root at the first
node on a branch was treated.
D I S C U S S I ON
This study has revealed new information on vascular
connections between root and parent and branch stolon at
a node (Fig. 3). The root connects with the lower nearside
axial bundle of the parent, and independently to lower and
SackŠille Hamilton and Hay—Vascular Architecture of Trifolium repens
upper nearside axial bundles of the branch (A4, A1« and A2«
for a node on the right as in Fig. 3). This last connection, at
the base of a branch, is the major link from roots to upper
axial bundles in well-branched plants, and resolves the
anomaly (see Introduction) that previous studies show no
connection from roots to upper axial bundles.
New information is also given on vascular connections to
the leaves on the first two nodes on a branch (Fig. 4). These
inevitably differ from those illustrated in Fig. 1 for nodes on
established stolons, because leaf traces arise up to two nodes
proximal to their corresponding leaf. The median trace of
the first leaf on a branch is unique in having a welldeveloped vascular connection to the root at the parent
node (Fig. 4 A), and therefore receives a large proportion of
its transpiration demand from that single nodal root, and
was consistently the most heavily dyed of all leaves on the
plant.
The upper trace of the second leaf on a branch arises from
the branch trace proximal to the point of insertion of the
root of the parent node. Thus the first trace to diverge from
the upper nearside axial bundle of a branch distal to the
point of insertion of the root of the parent node is the upper
trace of the fourth leaf (Fig. 4 B). This makes it a major sink
for the transpiration stream entering the upper nearside
axial bundle of a branch, and leads to a characteristic
feature, that no dye appears in the stipules of the first three
nodes of a branch whose parent root is supplied with dye,
while the fourth stipule is strongly dyed.
All pathways followed by the transpiration stream were
defined physically by the vascular bundles and their
interconnections. The pathway followed was variable,
depending on the distribution of sources (roots) and sinks
(leaves and other evaporative surfaces). The direction of
flow was usually acropetal, but could readily be reversed by
reversing the direction of the source-sink gradient. This is
consistent with the view that the vascular system is a passive
system of interconnected pipes.
Several aspects of the architectural features documented
here have implications for the intraplant distribution of
resources. For instance, the more numerous and larger
connections from the root to the branch as compared with
the parent stolon are consistent with results of $#P studies.
Where $#P was supplied to a nodal root of the same
genotype of ‘ Grasslands Kopu ’ at seven (Lo$ tscher and
Hay, 1996), ten (Chapman and Hay, 1993) or 12 (Hay and
Sackville Hamilton, 1996) nodes from the apex, $#P in the
branch at the node of the treated root was, respectively, 42,
50 and 63 % of the total $#P exported from the root. Similar
patterns occur in other genotypes : for example, in a genotype
from an old pasture in Wales, Kemball and Marshall (1994)
reported corresponding percentages of 27 and 71 % of the
$#P supplied to a nodal root eight and 12 nodes from the
apex, respectively.
Secondly, since a nodal root is connected only to nearside
axial bundles of both parent and branch stolons, roots at
the parent node of a branch and the (adjacent) first node on
that branch connect to the same lower axial bundle, whereas
the second node on the same branch connects to the
opposite lower bundle. Thus any tendency to basipetal flow
from the root on the first branch node would be counteracted
447
by acropetal flow from the root at the parent node. In this
study, basipetal flow from branch into parent was readily
induced from the root at the second node of the branch, but
not from that at the first node. In a related study (Hay and
Sackville Hamilton, 1996), there was a six-fold greater
basipetal movement of $#P into the parent stolon from a
treated nodal root on the farside rather than the nearside of
the branch.
Furthermore, it was clearly demonstrated that median
leaf traces were larger than lateral traces and were therefore
stronger sinks for the transpiration stream. Thus most of
the transpiration stream entering a leaf originated in the
lower sympodia supplying lower and median traces. The
lower axial bundles, therefore, supplied strong local leaf
sinks, while the upper axial bundles, supplying only upper
leaf traces, were found to transport dye throughout the
length of the branch stolon.
These results are largely consistent with the hypothesis
advanced to explain patterns of clonal integration observed
by Turkington et al. (1991). The lower axial bundles provide
a short-distance transport pathway to structures in close
proximity to the source root. It is suggested that this
pathway enables localized responses to favourable microsites to occur. In contrast, the upper axial bundles of a
branch provide a long-distance transport pathway from the
parent stolon to the apex of the branch stolon. It is
suggested that this pathway may enable high clonal
integration of exploratory growth at stolon apices to occur.
The generality of these results across other genotypes of
white clover has yet to be determined. Circumstantial
evidence is conflicting. On one hand, there is genetic
variation in the number of vascular bundles visible in crosssections of stolons, with larger-leafed varieties tending to
have more (Erith, 1924 ; Thomas, 1987). On the other hand,
$#P uptake studies using undisturbed plants have shown
similar patterns of distribution from root to parent and
branch stolons in 17 other genotypes of the same variety
‘ Grasslands Kopu ’ and in a morphologically-contrasting
small-leafed genotype ‘ Grasslands Tahora ’ (Lo$ tscher and
Hay, 1996, 1997).
The relevance of these studies to the field has yet to be
determined. The distribution of source-sink gradients in the
field is likely to be highly variable, and many nodes are
unrooted or unbranched. In addition, further studies are
required to clarify the role of other factors affecting clonal
integration, such as translocation in the phloem,
remobilization of nutrients, and utilization of resources
(Chapman and Robson, 1992). Nevertheless, the results
presented here are sufficient to demonstrate a functional
dichotomy between upper and lower axial bundles. This
may form the basis of a simple architectural mechanism to
explain the complex patterns of clonal integration that are
observed in T. repens, and may be a necessary part of
efficient foraging.
A C K N O W L E D G E M E N TS
The authors gratefully acknowledge the financial support
given by the British Council via its Higher Education Link
Scheme for this project. The first author thanks the Royal
448
SackŠille Hamilton and Hay—Vascular Architecture of Trifolium repens
Society for financial support. Professor R. G. Thomas,
Massey University, is thanked for his valuable comments
and advice. Figure 1 is reproduced by kind permission of the
Commonwealth Agricultural Bureau.
L I T E R A T U R E C I T ED
Chapman DF, Hay MJM. 1993. Translocation of phosphorus from
nodal roots in two contrasting genotypes of white clover (Trifolium
repens L.). Physiologia Plantarum 89 : 323–330.
Chapman DF, Robson MJ. 1992. Physiological integration in the clonal
perennial herb Trifolium repens L. Oecologia 89 : 338–347.
Devadas C, Beck CB. 1972. Comparative morphology of the primary
vascular systems in some species of Rosaceae and Leguminosae.
American Journal of Botany 59 : 557–567.
Erith AG. 1924. White cloŠer (Trifolium repens L.) : a monograph.
London : Duckworth & Co.
Hay MJM, Sackville Hamilton NR. 1996. Influence of xylem vascular
architecture on the translocation of phosphorus from nodal roots
in a genotype of Trifolium repens during undisturbed growth. New
Phytologist 132 : 575–582.
Hutchings MJ, de Kroon H. 1994. Foraging in plants : the role of
morphological plasticity in resource acquisition. AdŠances in
Ecological Research 25 : 159–238.
Kemball WD, Marshall C. 1994. The significance of nodal rooting in
Trifolium repens L. : $#P distribution and local growth responses.
New Phytologist 127 : 83–91.
Lo$ tscher M, Hay MJM. 1996. Distribution of mineral nutrient from
nodal roots of Trifolium repens : genotypic variation in intra-plant
allocation of $#P and %&Ca. Physiologia Plantarum 97 : 269–276.
Lo$ tscher M, Hay MJM. 1997. Genotypic differences in physiological
integration, morphological plasticity and utilization of phosphorus
induced by variation in phosphate supply in Trifolium repens.
Journal of Ecology 85 : 341–350.
Price EAC, Marshall C, Hutchings MJ. 1992. Studies of growth in the
clonal herb Glechoma hederacea. I. Patterns of physiological
integration. Journal of Ecology 80 : 25–38.
Roach WA. 1939. Plant injection as a physiological method. Annals of
Botany 3 : 155–226.
Thomas RG. 1987. The structure of the mature plant. In : Baker MJ,
Williams WM, eds. White cloŠer. Wallingford : CAB International,
1–29.
Turkington R, Sackville Hamilton NR, Gliddon CJ. 1991. Withinpopulation variation in localised and integrated responses of
Trifolium repens to biotically patchy environments. Oecologia 86 :
183–192.
Watson MA, Casper BB. 1984. Morphogenetic constraints on patterns
of carbon distribution in plants. Annual ReŠiew of Ecology and
Systematics 15 : 233–258.