New Phytol.

(1998), 138, 725–732

Cluster root development in Grevillea

robusta (Proteaceae)
I. Xylem, pericycle, cortex, and epidermis development in
a determinate root

B  K E I T H R. S K E N E*, J O H N A. R A V E N    J A N E T I. S P R E N T
Department of Biological Sciences, University of Dundee, Dundee DD1 4HN, UK
(Received 18 December 1996 ; accepted 19 November 1997)

(This paper is dedicated to the memory of Prof. Dr. Horst Marschner)


The cluster roots of Grevillea robusta A. Cunn. ex R. Br. are composed of determinate rootlets that stop growing,
but remain physiologically active for several months. Their apical organization, both before and after maturation,
was studied by light and transmission electron microscopy. Each cell layer forms a dome, with an initial cell at its
end. Xylem elements form a complicated triarch array at the base of the rootlet, passing along the rootlet as two
files, and then joining at the tip to form a single file, surrounded by six pericycle cells. At the base of the rootlet,
shorter xylem cells and thick-walled support cells are visible. A root cap, present in rootlets grown in vermiculite,
was eventually displaced by root hair growth. Rootlets grown in Hoagland’s solution lacked root caps and were
significantly shorter than those grown in vermiculite. Cell fate was analysed in terms of cell position and is
discussed in terms of pattern and development.

Key words : Grevillea robusta A. Cunn. ex R. Br., Proteaceae, meristem, determinate growth, cell fate.

members of the Proteaceae, a number of legumes,


It is thought that up to 30 % of the genome of
present-day vascular plants is involved in root system
development (Zobel, 1975). Roots not only provide
material for the investigation of this part of the
genome, but are also useful systems for looking at
basic questions of differentiation at a cellular level,
and morphogenesis at the level of the organ
(Schiefelbein & Benfey, 1991). Many unresolved
issues in root development are associated with the
root apex. The intricate work carried out on the
determinate root of Azolla (Gunning, 1978 ; Gun-
ning, Hughes & Hardham, 1978 a ; Gunning,
Hardham & Hughes, 1978 b) gave an insight into the
fate of cells following division.
Cluster roots consist of dense clusters of rootlets of
determinate development, arising endogenously
from the pericycle of lateral roots, opposite prot-
oxylem poles (Purnell, 1960). They occur in most
* To whom correspondence should be addressed.
E-mail : k.r.skene!dundee.ac.uk
and in members of the Casuarinaceae, Myricaceae,
Betulaceae and Moraceae, and are thought to be
involved in phosphate acquisition (for references see
Dinkelaker, Hengeler & Marschner (1995)). In
Grevillea robusta they are produced at set distances
along lateral roots (Skene et al., 1996), and are
thought to improve the acquisition of phosphate and
other nutrients (Dinkelaker et al., 1995). These roots
are a useful system for studying root initiation and
development. Firstly, the sites of their initiation can
be precisely located before initiation, thus allowing
the earliest stages in root development to be
investigated. Such predictive certainty has long been
sought after (e.g. Mallory et al., 1970 ; Charlton,
1983 ; Hinchee & Rost, 1992 ; Newson, Parker &
Barlow, 1993). Secondly, the determinate nature of
development in the rootlets that make up the clusters
allows cell fate to be followed to its ultimate
conclusion.
Determinate roots fall into six categories. Firstly,
there are those that become ‘ determinate ’ owing to
damage inflicted on their meristems (Varney &

726 K. R. Skene, J. A. Raven and J. I. Sprent
McCully, 1991) either from biotic or abiotic sources.
Secondly, symbiotic relations can lead to the pro-
duction of determinate roots such as in certain
mycorrhizas (Harley & Smith, 1983 ; Fitter, 1985 ;
Berta et al., 1990) and in actinomycete infections of
Myrica, Casuarina and Comptonia (Torrey &
Callahan (1978) and references therein). Thirdly,
some species seem to undergo a programmed
abscission of the apical meristem, such as in the
water fern Azolla (Gunning, 1978), Zea (Fusseder
1987 ; McCully, 1987 ; Cahn, Zobel & Bouldin,
1989 ; Varney & McCully, 1991) and Allium (Berta et
al., 1990). Root thorns in palms fall into this category
(McArthur & Steeves, 1969). Fourthly, some roots
appear determinate, but are in fact dormant (Varney
& McCully, 1991, Couot-Gastelier & Vartanian,
1995). Fifthly there are roots whose meristem
undergoes differentiation but in which there is no
abscision. The determinate roots of Opuntia arenaria
(Boke, 1979) fall into this category. Finally, there are
roots in which, after a period of apical growth, the
meristem itself differentiates, but the tip remains
intact and physiologically active. Cluster rootlets are
the definitive example. In G. robusta, the rootlet
grows for a period, then the meristem differentiates
and at this point root hairs are formed (Skene et al.,
1996). Following this, exudation of organic acids
begins (H. Marschner, pers. comm.).
The aim of this study was to examine the
implications of determinate growth on tissue organ-
ization at the tip of the root, with emphasis on
epidermis, cortical layers, pericycle and xylem. A
similar study of the endodermis is reported in a
subsequent paper (Skene et al., 1998).
  
Plant material
Grevillea robusta A. Cunn. ex R. Br. seedlings
(Provenance Loitokitok, Kenya Forestry Seed
Centre) were grown in Vermiperl2 (medium grade
from William Sinclair Hort. Ltd., Firth Road,
Lincoln, UK)}Silvaperl2 (graded horticultural per-
lite from Silvaperl Ltd., Albion Works, Ropery
Road, Gainsborough, Lincs., UK) (3 : 1), under
controlled conditions (Skene et al., 1996). Following
16 wk of growth on vermiculite, plants were ex-
amined for the presence of cluster roots. Over 2000
sections were examined, taken from 12 plants and 48
cluster roots (four from each plant).
Light microscopy
Cluster roots were placed in 4 % glutaraldehyde in
phosphate buffer (1 : 1 KH PO (50 mmol dm−$) :
# %
K HPO (50 mmol dm−$), pH 6±8) at 2 °C for 24 h.
# %
Specimens were rinsed twice in buffer for 1 h, then
postfixed in 0±2 % OsO (w}v) in buffer for 24 h. The
%
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roots were then embedded in 1 % agar. Blocks were
trimmed in the desired orientation before being
taken through an ethanol series (30, 40, 50, 60, 70, 80
and 90 %, made up in distilled water), followed by
two rinses in 100 % ethanol, for 30 min at each stage.
Blocks were placed in L. R. White2 resin (London
Resin Company) 1 : 1 (v}v) in absolute alcohol,
vacuum infiltrated and rotated at 2 °C for 24 h,
before being transferred to 100 % L.R. White resin,
changed every 2 d, for 6 d. They were then placed in
gelatine capsules which were filled with resin and left
to polymerize at 60 °C for 24 h. They were sliced at
1 µm thickness using a Reichert2 (OM U3) micro-
tome with a glass knife, and stained with 33 mmol
dm−$ toluidine blue in 162 mmol dm−$ sodium
tetraborate before viewing with an Olympus2 BH2
microscope.
Transmission electron microscopy (TEM)
Specimens were prepared as for light microscopy.
Sections of 90 nm thickness were taken and placed
on pyroxylin copper grids (50 mesh). Sections were
stained for 30 min with uranyl acetate, and for
10 min with lead citrate, at room temperature. They
were viewed and photographed using a JEOL2
1200EX transmission electron microscope.

Differentiation of apical region
The root cap in developing cluster rootlets is only
one layer thick (Fig. 1 a). As the meristem itself
differentiates, some of the epidermal cells become
trichoblasts, and their hairs push through the root
cap layer (Fig. 1 b). In mature rootlets, each cell layer
differentiates up to its initial (Figs 1 b, c, 2 f ). The
cortical cells are packed with starch granules at all
levels of the rootlets (Figs 1 c, 2 b), except in old
rootlets (Fig. 2 f ). At the base of the rootlets there is
a complicated array of xylem vessels (Fig. 2 a),
forming part of the vascular junction complex (VJC).
In transverse sections, the VJC is triarch, with two
arms pointing towards the parent root apex (Fig.
2 a). Above the VJC, two columns of xylem elements
continue towards the apex of the rootlet (Fig. 2 b). At
the apex, these elements join to form a single file of
xylem cells, surrounded by six pericycle cells (Fig.
2 c). Nearer the apex, the pericycle cells form a dome
(Figs 1 b, 2 d ). At this stage, large intercellular
spaces, containing osmiophilic material (Fig. 2 e) are
visible between the pericycle cells. The endodermis
initial differentiates, surrounded by six endodermal
cells, six inner cortical cells and 12 outer cortical
cells (Fig. 2 f ). In transverse sections, these six cells
are not always visible, owing to differences in their
spatial arrangement. Development of the apex is
consistent, regardless of the growth medium.
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Tissue development in cluster roots 727

(a)

(b) (c)

Figure 1. The apex of a cluster rootlet in Grevillea robusta. (a) Median longitudinal section (MLS) through
the apical region of a growing cluster rootlet just completing growth. Ci, inner cortex ; Co, outer cortex ; Ep,
epidermis ; En, endodermis ; Pe, pericycle ; R, root cap ; Th, thickened wall. Bar, 25 µm. (b) LM, L.S. Mature
cluster rootlet with root hairs (RH) growing through root cap. Bar, 50 µm. (c) LM, L.S. Mature cluster rootlet.
The terminal xylem cell is visible (X) between two pericycle cells. Bar, 50 µm.

In Figure 3 a–d, it can be seen that the junction
complex is made up of more rotund, shorter cells at
the base, connecting the rootlet xylem to the parent
xylem. At the centre of this complex, these shorter
cells are surrounded by thick-walled cells, but
without thickened banding (Fig. 3 b). These shorter
cells have differentiated from stelar parenchyma cells
and from cells originating from the primordium of
the rootlet (Fig. 3 c). They form multiple connections
between the parental and rootlet xylem. In Figure
3 d, the dark-staining endodermal cells of the rootlet
can be seen, with two short xylem cells (s) visible.
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728 K. R. Skene, J. A. Raven and J. I. Sprent

(a) (b)

(c) (d )

(e) (f )

Figure 2. Changes in the central stele in a cluster rootlet in Grevillea robusta. (a) L.S. of parent root, through
the vascular junction complex, just above the parent vascular tissue. The parent root apex lies to the right.
Xylem elements (X) are triarch. Bar, 12 µm. (b) T.S. near the centre of a cluster rootlet. Two xylem elements
are visible (X). Note also three dense cells in the pericycle layer (dp). Ep, epidermis ; En, endodermis ; RH, root
hair ; p, phloem. Bar, 12 µm. (c) T.S. near apex, showing a single xylem cell surrounded by six pericycle cells.
Bar, 10 µm. (d ) T. S. slightly more apical than 2C, six pericycle cells, surrounded by the endodermis, are visible.
(e) TEM, T.S. at a position nearer the apex than (d ). Notice the intercellular space (IS). Three pericycle cells
(P) are visible. Bar, 2 µm. (f ) T.S. of an older cluster root sectioned through the endodermal initial (EnI). Note
four of the six final endodermal derivatives (End), six inner cortical cells (Ci) and 12 outer cortical cells (Co).
Bar, 10 µm.
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Tissue development in cluster roots 729

(a) (b)

(c) (d)

Figure 3. Cluster root junctions. (a) T. S. through parent root at junction, showing shorter, basal xylem cells
(s) below longer cells (l). Bar, 10 µm. (b) T.S. through parent root at the centre of a junction, showing thickened
supporting cells (T) on either side of the shorter xylem cells (s) with longer xylem cells (l). Bar, 10 µm. (c) L.
S. of a parent root in the upper region of a junction, showing the mass of shorter xylem cells (s). Bar, 30 µm.
(d ) T.S. through the lower part of a cluster root junction, showing endodermal cells (En), and small xylem cells
(s) at the base of the xylem. Bar, 10 µm.

Rootlet length and density were compared under
growth in vermiculite and hydroponics. Measuring
rootlets from 50 cluster roots grown in each medium,
showed that those growing in Hoagland’s solution
were significantly shorter (1±54³0±51 mm ()) than
those grown in vermiculite (3±05³0±48 mm) while
there was no significant difference on rootlet density
(191³25 cm−") for rootlets grown in vermiculite,
compared with 189³25 cm−" for rootlets grown in
Hoagland’s solution.
Positions of individual cells were determined in
terms of neighbouring cell types (Table 1). A cell of
a given cell type can lie adjacent to different types of
cells (in the case of mature rootlets), or cells that will
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730 K. R. Skene, J. A. Raven and J. I. Sprent

Table 1. Cell fate and neighbouring cell types in cluster roots

Neighbours

Cell description External Internal Radial Fate

Pericycle initial EnI X Pe, En Pericycle

Pericycle derivative 1 En X PeI, Pe Pericycle
Pericycle derivative 2 En Stele Pe Pericycle
Endodermal initial CIi PeI En, Ci Endodermis
Endodermal derivative 1 Ci PeI EnI, En Endodermis
Endodermal derivative 2 Ci Pe En Endodermis
Inner cortex initial CIo EnI Ci, Co Inner cortex
Inner cortex derivative 1 Co En CIi, Ci Inner cortex
Inner cortex derivative 2 Co En Ci Inner cortex
Outer cortex initial EpI CIo Co, Ep Outer cortex
Outer cortex derivative 1 Ep Ci CIo, Co Outer cortex
Outer cortex derivative 2 Ep Ci Co Outer cortex

The different cell types adjacent to cells of a particular cell type are listed,
allowing comparisons of cell fate and position in terms of neighbours. Ci, inner
cortex ; Co, outer cortex ; En, endodermis ; Ep, epidermis ; EnI, endodermal
initial cell (other innitial cells indicated likewise) ; Pe, pericycle ; X, xylem.

differentiate into different types of cells (in immature
rootlets). However, in every case a cell of a given cell
type shared a radial wall with a cell of that type.

The interpretation of micrographs can be difficult,
especially in the case of root apices. We have used
both transverse and longitudinal serial sections in an
attempt to build a true picture of events, as
recommended by Clowes (1994). Cluster rootlets in
Grevillea robusta are determinate (Purnell, 1960,
Skene et al., 1996). There is a closed meristem, and
while active, it appears to be composed of a single
tier of cells (Fig. 1 a). The same arrangement has
been reported for primary roots of G. robusta
(Hejnowicz (1980) in Barlow (1995)), although there
are differences in the number of cell layers observed.
Such conservation of tiers is of interest, considering
the great differences in size, longevity and function
between roots. Presence or absence of a quiescent
centre in young cluster rootlets of G. robusta has yet
to be confirmed, but appears to be absent.
The root cap in developing cluster roots of G.
robusta, is a single layer thick (Fig. 1 a). The
epidermis might not be completely discrete, but with
root cap and epidermis originating from the same
initial, although a thicker wall exists between
epidermis and root cap than between other layers
(Fig. 1 a). The cells of the two layers, although not
identical, exhibit alignment of anticlinal wall position
in many locations. We do not agree with Barlow
(1995) that the thicker wall between these layers is
evidence of a separate initial.
It can be seen that the various cell layers
differentiate acropetally, and the cylinders of tissues
form domes at the apex, centred around the initial
cells. Eight-sided cells are the typical structural
initial in gymnosperm and angiosperm roots (Barlow
1994). In Figure 2 f, this older rootlet displays the
geometry of the apex very clearly. The initial cells
each have six faces from which derivative cells are
produced, and these cells then undergo division.
There are no divisions along the upper and lower
faces of these initials, except for the lower face of the
basal initial (forming xylem and other stelar initials),
and the upper face of the most apical initial (to form
the root cap).
Pattern
For almost 200 yr, scientists have endeavoured to
understand what leads to particular developmental
patterns (Byrne (1974) and references therein). What
light does this present study shed on the elucidation
of the cause of pattern ? The idea of a predetermined
pattern set in the meristem would certainly explain
the events observed at the apex. If each of the initial
cells produced derivatives that were fated to a
particular destiny, one would expect each cell layer
to differentiate as a dome. However this explanation
cannot account for the events at the junction of the
rootlet with the parent root, as described for the
endodermis (Skene et al., 1998), and the xylem (this
study), since cells in this region re-differentiate.
Furthermore, since the epidermis and root cap arise
from the same initial, something else must determine
their separate destinies. Berg et al. (1995), in a laser
ablation experiment, concluded that cell fate within
an individual cell layer is propagated through that
layer from base to tip, in a ‘ feed-forward cuing ’
(Lang, 1965 ; Gunning et al., 1978 b). This ex-
planation would again appear to explain events at the

Tissue development in cluster roots
apex. Table 1 shows that a cell destined for one fate
always shares this destiny with at least one of its
radial associates. For example, if we look at the
pericycle cells in Table 1, the one common neighbour
of both initial, first derivative and second derivative
cells is another pericycle cell in a radial position. The
same applies to endodermis, inner cortex and outer
cortex. If cells communicated via these radial walls
alone, then this could explain the observed pattern.
However, basal events would require some fine-
tuning of this mechanism, as there are more xylem
cells in the lower stele, and the endodermis under-
goes a 90° change in direction at the junction (Skene
et al., 1998). The idea of the cell wall maintaining the
differentiated state and directing cell fate (Berger,
Taylor & Brownlee, 1994) also runs into difficulties
at the root junction level.
Could the fate of any one cell be determined by the
combined effect of all of its neighbours ? Table 1
demonstrates that one cell type can be surrounded
by different sets of neighbouring cell types. Thus if
each cell plays a role in determining the fate of
another cell, it is certainly not a simple relationship.
However, in terms of re-differentiation, this ex-
planation could function in terms of a changing
neighbourhood leading to a new fate, but it cannot
account for the events leading up to initiation. Any
idea of a supracellular, morphogenetic field might
merely be an elaboration of this ‘ nearest neighbours ’
explanation.
Rootlet junctions
Cluster roots (and, indeed, all lateral roots in
angiosperms) have complex junctions with parent
roots (Skene et al., 1998). This is necessitated by the
way they develop, from a cell layer sandwiched
between parental xylem and parental endodermis.
Thus, the parental endodermis must undergo a
linkage process with the rootlet endodermis that
involves re-differentiation of rootlet cortical cells.
This means that the simple ‘ up-down ’ communi-
cation between mature daughter cells and initials
(Berg et al., 1995) cannot be the only process
involved, and ‘ sideways ’ conversation must take
place as well. The same would appear to be true in
xylem differentiation at the base of a root, where
stelar parenchyma re-differentiates as xylem cells
(Byrne, Pesacreta & Fox, 1977 ; Byrne, Byrne &
Emmitt, 1982). In Figure 3, the arrangement of cells
at the base of the rootlet is highly organized,
involving several cell types, including thick-walled
cells, positioned on either side of the xylem.
Although the meristem might not determine the fate
of a particular cell, cell division results in files of cells
that eventually differentiate in the same way. The
order of the mature cluster rootlet tip reflects
previous order in cell divisions within the meristem.
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731
If a given cell is a derivative of an endodermal initial,
it will become an endodermal cell (unless ablated
(Berg et al., 1995) !).
The cell itself can be defined by position (Barlow,
1984 ; Steeves & Sussex, 1989 ; Irish, 1991 ; Berg et
al., 1995), but we must ask if the position is defined
by the clonal origin of neighbouring cells. As long
ago as 1952, Bunning (in Clowes (1961)), cut off the
apical 2 mm of roots, rotated and replaced them, and
found that the new vascular tissue in the tip was out
of line with that in the stump. Torrey (1955) (in
Clowes (1961)) also found the meristem of Pisum
could impose an influence on the root. Taking both
basal and apical development, it can be seen that
patterns do exist, but the elucidation of their origin
is complicated.
Determinate growth
The determinate nature of cluster rootlet devel-
opment clearly merits consideration. Since cortical
cells at the apex of mature rootlets are packed with
starch (Figs 1 c, 2 b, c), it seems unlikely that the
meristems are starved into differentiation. This
situation might therefore differ from that in Azolla
(Gunning, 1978), where a reduction in numbers of
plasmodesmata might gradually isolate the meristem
(but see van Bel & Oparka (1995) on drawbacks of
plasmodesmatal counts), but here, the root tip often
abscises eventually. In the cluster root, rootlets
remain physiologically active, in that a globular
exudate is not released from the epidermis until
determination (Skene et al., 1996). In old rootlets
(30 d after initiation), cortical cells have few starch
granules (Fig. 2 f ). The starch might have been
metabolized in non-growth-related activities, indi-
cating continued physiological activity.
Cluster roots are ellipsoid in shape, with rootlets
on the extreme edges smaller than those in the
centre. Thus the determinate nature of each rootlet
is related to a bigger pattern between rootlets, and
seems to be controlled at a parent-root level. A factor
influencing their length might be related to the
gradient (or gradients) of a substance (or substances)
along the parent root, as suggested by Barlow (1976).
              
This work was funded by NERC. Thanks to Margaret
Gruber (photography), Martin Kierans (microscopy) and
Shona McInroy (technical assistance). We are grateful to
Dr Joan Sutherland for helpful discussion. We acknowl-
edge the helpful comments of three anonymous referees.
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