Annals of Botany 87: 649±654, 2001
doi:10.1006/anbo.2001.1385, available online at http://www.idealibrary.com on
Epidermal Patterning in Seedling Roots of Eudicotyledons
L I A M . S. P E M B E R TO N , S H I N - L I N G T S A I , P E T E R H . LOV E L L and P H I L I P J . HA R R I S *
School of Biological Sciences, The University of Auckland, Private Bag 92019, Auckland, New Zealand
Received: 2 November 2000
Returned for revision: 17 December 2000 Accepted: 22 January 2001 Published electronically: 27 March 2001
Three types of epidermal patterning occur in roots of angiosperms: in Type 1, all the epidermal cells can potentially
produce root hairs (hair cells); in Type 2, asymmetric cell divisions produce short cells that develop into hair cells and
larger cells that do not (non-hair cells); and in Type 3, hair cells occur in ®les separated by one to three ®les of non-hair
cells. In the present study we examined the epidermal patternings of seedling roots of 77 eudicotyledonous species from
43 families. We found that Type 1 patterning was the most common and no species had Type 2 patterning. Previously,
Type 3 epidermal patterning had been described only in the family Brassicaceae. In addition to the Brassicaceae
(including the Capparaceae), we found Type 3 patterning in the Brassicales families Limnanthaceae and Resedaceae,
whereas the other Brassicales families we examined, Caricaceae and Tropaeolaceae, had Type 1 patterning. We also
found Type 3 patterning in six families of the Caryophyllales sensu lato: Amaranthaceae, Basellaceae,
Caryophyllaceae, Plumbaginaceae, Polygonaceae and Portulacaceae. However, the family Cactaceae, which is also
in this order, had Type 1 patterning. Only one other species, Nemophila maculata (Boraginaceae), had Type 3
patterning; the other two species that we examined in this family had Type 1 patterning. Type 3 patterning thus occurs
# 2001 Annals of Botany Company
more widely in the eudicotyledons than was previously thought.
Key words: Brassicales, Caryophyllales, eudicotyledons, epidermal patterning, phylogeny, root hairs, roots, seedlings.
I N T RO D U C T I O N
Root epidermal cells make up the outermost layer of a root
and can give rise to root hairs which are tubular outgrowths
from these cells. Root hairs are important in aiding the
uptake of nutrients and water and anchoring the plant in the
soil by greatly increasing the surface area of the root (Hofer,
1996; Peterson and Farquhar, 1996; Ridge, 1996; Gilroy and
Jones, 2000). Two types of epidermal cells can be recognized: those which develop a root hair (hair cells), and those
which remain hairless (non-hair cells). In angiosperms, the
hair and non-hair cells are arranged in three types of
patterns (Dolan and Roberts, 1995; Dolan, 1996). In Type 1
patterning, all the root epidermal cells have the potential to
produce root hairs, although this potential is not always
realized. Except for the presence of hairs, these hair cells do
not appear to be morphologically di€erent from non-hair
cells. Type 2 patterning is characterized by asymmetric cell
divisions of the epidermal cells in the meristematic zone. A
root hair develops from the smaller of the two cells produced
by this division; the larger cell remains hairless. In Type 3
patterning, the hair cells occur in ®les separated by one to
three ®les of non-hair cells. The number of ®les of non-hair
cells was shown to be ecotype-dependent in the roots of
Arabidopsis thaliana (Berger et al., 1998). In this species, the
hair cells are also shorter than non-hair cells and have denser
cytoplasm (Dolan et al., 1993, 1994).
The distribution of these di€erent types of root-epidermal
patternings in di€erent angiosperm taxa has only been
investigated to a limited extent (Dolan and Roberts, 1995;
Dolan, 1996). Type 1 patterning appears to be the most
* For correspondence. Fax ‡64-373-9-7416, e-mail p. harris@
auckland.ac.nz
0305-7364/01/050649+06 $35.00/00
widespread. Leavitt (1904) carried out a large survey of
angiosperms and found Type 2 patterning in some families
of monocotyledons, including the Poaceae, and in the
dicotyledonous family Nymphaeaceae, but not in any of the
families now known as the eudicotyledons (Angiosperm
Phylogeny Group, 1998). Types 1 and 2 were also found in
the Poaceae by Row and Reeder (1957). Type 3 patterning
was ®rst described by Cormack (1935) in the brassicaceous
species Brassica oleracea, B. alba (ˆSinapis alba), B. napus
var. chinensis (ˆB. chinensis) and Raphanus sativus, and has
since been found in two other species in this family:
Lepidium sativum (BuÈnning, 1951) and the model plant
Arabidopsis thaliana (Dolan et al., 1993, 1994). Cao et al.
(1999) stated: `This cellular organisation of the root
epidermis is a characteristic of most members of the
Brassicaceae and has not to our knowledge been described
for species outside this family'. In his survey of angiosperms,
Leavitt (1904) recognized only Type 1 and 2 patternings.
Type 3 patterning was probably overlooked at that time and
recorded as Type 1. Indeed, Leavitt (1904) recorded two
species of Brassicaceae, Cardamine hirsuta and Nasturtium
ocinale (ˆRorippa nasturtium-aquaticum), as having Type
1 patterning. It is thus possible that Type 3 root-epidermal
patterning occurs in angiosperm taxa other than the
Brassicaceae, but has not been recognized to date. Further
indirect evidence for this view was presented by Clowes
(2000). His anatomical study of root apical meristems
showed that trichoblasts ( precursors of hair cells) were
arranged in a radial pattern in many families, including
several families in the Brassicales. This type of trichoblast
distribution could lead to a Type 3 pattern of root hairs.
In the present study we examined the root-epidermal
patterning of seedlings of 77 species in 43 families of
# 2001 Annals of Botany Company
650
Pemberton et al.ÐRoot Epidermal Patterning
eudicotyledons, including 17 species of the family Brassicaceae. In planning this survey, we used the Angiosperm
Phylogeny Group (1998) classi®cation of angiosperms
which is mostly based on recent molecular phylogenetic
analyses.
M AT E R I A L S A N D M E T H O D S
Plant materials
Four seeds of 77 species of eudicotyledons in 43 families
were placed on two pieces of ®lter paper (No. 1, Whatman
Ltd, Maidstone, UK) in 90 mm diameter glass Petri dishes.
Sterilized distilled water (3 ml) was added to the Petri
dishes, which were sealed with Para®lm M1 (American Can
Company, Greenwich, CT, USA) to prevent water loss, and
placed in the dark at 25 8C until the primary roots were up
to 40 mm long. Seeds of the few species that did not germinate under these conditions were sown in 100 mm diameter
pots in steam sterilized general potting mix (Watkins,
Onehunga, Auckland) and kept at 23±25 8C in a glasshouse
with natural lighting until the seeds had germinated and the
primary roots were up to 60 mm long. The seedlings were
removed from the ®lter paper or potting mix and excess soil
was removed by gently washing with water.
Microscopy
Bright-®eld microscopy. The primary roots were cut,
using a scalpel, from three to ®ve seedlings of each species,
stained and examined by bright-®eld microscopy using a
Zeiss KF2 microscope (Oberkochen, Germany) ®tted with
a 20 W halogen quartz lamp; the type of epidermal
patterning was recorded. When we started the survey, we
stained roots in 0.05 % aqueous Toluidine Blue for 1 min,
and then rinsed o€ excess stain. However, we later found
that clearer results were obtained by staining the roots for a
few seconds in black ink (Pelikan 4001, Brilliant Black,
Germany) and removing excess ink with wet ®lter paper.
Scanning electron microscopy (SEM). Roots of
L. douglasii seedlings were used 3 d after emergence
(approx. 40 mm long). Roots were cut 5 to 7 mm from
the root tip, using a scalpel, and were stuck as quickly as
possible with carbon tape onto an SEM stub. The root tips
were then frozen by plunging them into a nitrogen slush.
Preliminary work, with no partial freeze drying of the
specimens, showed that there was a problem with ice
crystals that formed on the surfaces of the roots and root
hairs. To reduce the occurrence of these ice crystals, the
stub was heated for 5 min to ÿ85 8C at 0.05 Torr in a
special workchamber (Model SP2000, Emscope, Kent, UK)
to allow the water to sublime. The stub was coated with
gold under vacuum at ÿ185 8C using a sputter coater
(Emscope) and inserted onto the cold stage of a scanning
electron microscope (Model 505, Philips, Eindhoven, The
Netherlands). Microscopy was done at 12 kV with the stage
at ÿ185 8C. Photographs were taken on Ilford Plus
125-FP4 black and white ®lm. The negatives were scanned
(Leafscan 45, Scitex, Massachusetts, USA) and the images
imported into Adobe Photoshop2 (Adobe Systems Inc.,
Mountain View, CA, USA).
R E S U LT S
The type of root-epidermal patterning of the seedling
eudicotyledon species examined is shown in Table 1. Type 1
epidermal patterning was found in the majority of species,
whereas Type 3 occurred only in the orders Brassicales and
Caryophyllales sensu lato, and the family Boraginaceae.
Type 2 root-epidermal patterning was not found in any of
the species examined.
In the Brassicales, all 17 species examined from 17 genera
of the Brassicaceae had Type 3 root-epidermal patterning.
These included Cleome spinosa, which was formerly placed
in a separate family, the Capparaceae, but is now placed in
the Brassicaceae (Angiosperm Phylogeny Group, 1998).
Four other families of Brassicales were studied: Limnanthaceae, Resedaceae, Caricaceae and Tropaeolaceae. Type 3
patterning was found in Limnanthes douglasii (Limnanthaceae) and in Reseda alba and R. odorata (Resedaceae), but
Type 1 patterning was present in Tropaeolum majus and
T. peregrinum (Tropaeolaceae) and Carica papaya (Caricaceae). The root-epidermal patterning of seedlings of
Limnanthes douglasii was examined by SEM as an example
of a species from a family other than the Brassicaceae which
we found, using bright-®eld light microscopy, had Type 3
patterning. This patterning is shown in Fig. 1. In the
Caryophyllales sensu lato, Type 3 root-epidermal patterning
was present in all the species examined except Mammillaria
leucocentra (Cactaceae), which had Type 1 patterning
(Table 1). The seedlings of this species had short, slowly
elongating primary roots with extremely long hairs arising
close to the apex. These long root hairs could be a
compensating mechanism for successful seedling establishment in xerophytic conditions. Only one other species had
Type 3 root-epidermal patterning: Nemophila maculata in
the Boraginaceae (including the Hydrophyllaceae), a family
in the Euasterids I not yet placed in an order (Angiosperm
Phylogeny Group, 1998).
F I G . 1. Scanning electron micrograph of the surface of a seedling root
of Limnanthes douglasii (Limnanthaceae) in the zone of root-hair
elongation. The hair cells are in ®les separated by one or two ®les of
non-hair cells, indicating Type 3 patterning. Bar ˆ 100 mm.
Pemberton et al.ÐRoot Epidermal Patterning
651
T A B L E 1. The root-epidermal patterning types of the seedlings examined. The taxa are classi®ed according to the Angiosperm
Phylogeny Group (1998)
Taxa examined
EUDICOTS
Ranunculales
Papaveraceae
Papaver nudicaule L.
Ranunculaceae
Aquilegia vulgaris L.
Nigella damascena L.
CORE EUDICOTS
Caryophyllales
Aizoaceae
Dorotheanthus bellidiformis (Burm. f.) N.E. Br.
Amaranthaceae
Amaranthus tricolor L.
aAtriplex hortensis L.
Celosia argentea var. cristata (L.) Kuntze
Gomphrena globosa L.
aSpinacia oleracea L.
Basellaceae
a
Basella rubra L.
Cactaceae
b
Mammillaria leucocentra Berg.
Caryophyllaceae
Dianthus caryophyllus L.
Plumbaginaceae
Limonium sinuatum (L.) Mill.
Polygonaceae
Rumex acetosa L.
Portulacaceae
Calandrinia umbellata (Ruiz & Pav.) DC.
Claytonia perfoliata Donn ex Willd.
ROSIDS
Geraniales
Geraniaceae
Pelargonium hortorum L.H. Bail.
EUROSIDS I
Cucurbitales
Cucurbitaceae
Cucurbita moschata Duchesne ex Poir.
Fabales
Fabaceae
Trifolium repens L.
Malpighiales
Euphorbiaceae
c
Drypetes deplanchei subsp. anis Pax & K. Ho€m.
Euphorbia variegata De¯ers
Linaceae
Linum usitatissimum L.
Passi¯oraceae
aPassi¯ora edulis Sieber ex Sims
Violaceae
Viola tricolor L.
Rosales
Rosaceae
Geum chiloense Balb. ex Ser.
EUROSIDS II
Brassicales
Brassicaceae
Arabidopsis thaliana (L.) Heynh. ecotype Columbia
Barbarea verna (Mill.) Asch.
Brassica oleracea L.
Cleome spinosa Jacq.
Eruca sativa (Mill.) Thel.
Erysimum cheiri (L.) Cranz.
Hesperis matronalis L.
Iberis umbellata L.
aIsatis tinctoria L.
Lepidium sativum L.
Lobularia maritima (L.) Desv.
Lunaria annua L.
Malcolmia martima (L.) R. Br.
Matthiola bicornis (Sm.) P. Ball
Raphanus sativus L.
Rorippa nasturtium-aquaticum (L.) Hayek
Sinapis alba L.
a
Patterning type
1
1
1
3
3
3
3
3
3
3
1
3
3
3
3
3
1
1
1
1
1
1
1
1
1
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
3
Seeds germinated in potting compost.
Roots 2 mm long when sampled.
c
Roots taken from a mature plant growing in potting compost.
b
Taxa examined
Caricaceae
a
Carica papaya L.
Limnanthaceae
Limnanthes douglasii R. Br.
Resedaceae
Reseda alba L.
R. odorata L.
Tropaeolaceae
a
Tropaeolum majus L.
aT. peregrinum L.
Malvales
Malvaceae
Althea ocinalis L.
Hibiscus esculentus L.
a
Lavatera trimensis L.
a
Malva sylvestris L.
aSidalcea malvi¯ora (DC) Benth.
Myrtales
Onagraceae
aFuchsia denticulata Ruiz & Pav.
Oenothera glazioviana Micheli ex Mart.
Sapindales
Rutaceae
aRuta graveolens L.
ASTERIDS
Ericales
Balsaminaceae
Impatiens walleriana Hook. f.
Polemoniaceae
Phlox drummondii Hook.
Primulaceae
a
Primula veris L.
EUASTERIDS I
Boraginaceae
Echium plantagineum L.
Phacelia campanularia A. Gray.
Nemophila maculata Benth.ex Lindl.
Gentianales
Apocynaceae
aAsclepias curassavica L.
Rubiaceae
Asperula orientalis Boiss & Hohen.
Lamiales
Bignoniaceae
a
Eccremocarpus scaber Ruiz & Pav.
Lamiaceae
Perilla frutescens var. crispa (L.) Britt.
Scrophulariaceae
Antirrhinum majus L.
Verbenaceae
a
Verbena venosa Gill. & Hook.
Solanales
Convolvulaceae
Convolvulus minor L.
Solanaceae
Lycopersicon esculentum Mill.
Nolana paradoxa Lindl.
EUASTERIDS II
Apiales
Apiaceae
Daucus carota L.
Asterales
Asteraceae
Echinops ritro L.
Helianthus annuus L.
Lactuca sativa L.
Campanulaceae
Campanula persicifolia L.
Dipsacales
Dipsacaceae
Scabiosa stellata L.
Valerianaceae
a
Valeriana ocinalis L.
Patterning type
1
3
3
3
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
3
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
652
Pemberton et al.ÐRoot Epidermal Patterning
Type 3 patterning varied slightly among the species
examined: hair ®les and non-hair ®les alternated, for
example in Raphanus sativus; one or two non-hair ®les
occurred between the hair ®les, for example in Basella
rubra, Calandrinia umbellata and Limnanthes douglasii; and
two or three non-hair ®les occurred between the hair ®les in
Nemophila maculata, Reseda alba and R. odorata. We also
found the rare occurrence of two adjacent hair ®les in the
seedling roots of Spinacia oleracea. The epidermal patterning on the roots of seedlings of Limnanthes douglasii with
hair ®les separated by one or two non-hair cell ®les is shown
in Fig. 1.
DISCUSSION
In our survey of seedling roots of eudicotyledons, epidermal
patterning was either Type 1 or 3, with Type 1 being the most
common; Type 2 patterning was not found, which is consistent with the survey of Leavitt (1904). Type 3 patterning
occurred only in the orders Brassicales and Caryophyllales
sensu lato, and in Nemophila maculata, which is a member of
the Boraginaceae, a family in the Euasterids I not yet placed
in an order (Angiosperm Phylogeny Group, 1998). In the
Brassicales, all species examined within the family Brassicaceae had Type 3 epidermal patterning, including Rorippa
nasturtium-aquaticum, which was described as Type 1 by
Leavitt (1904). The Brassicaceae is a large, homogeneous
family with 365 genera and 3250 species (Mabberley, 1997);
it is thus likely that all the species have this type of epidermal
patterning.
We found Type 3 patterning in other families of the
Brassicales; this is the ®rst time this type of patterning has
been described outside the Brassicaceae. Furthermore, the
other families within the Brassicales that have Type 3
patterning appear phylogenetically to be the most closely
related to the Brassicaceae. The phylogeny of families within
the Brassicales has been investigated using morphological
characters and the nucleotide sequences of rbcL and 18 S
nrDNA (Rodman et al., 1996, 1998). A cladogram
constructed by combining DNA sequence data from these
two genes is shown in Fig. 2. The families we examined that
have Type 3 patterning are present only in a subclade of the
main Brassicales clade comprising species that have an
extension to the 30 end of the rbcL gene and which does not
occur elsewhere in the Brassicales. This subclade, which
includes all the Brassicales families other than the Akaniaceae, Bretschneideraceae, Caricaceae, Moringaceae and
Tropaeolaceae, is also synapomorphic for two morphological characters: onagrad embryogeny and dilated cisternae of
the endoplasmic reticulum, which are unique to this clade
(Rodman et al., 1998). The families that have Type 1
patterning, Caricaceae and Tropaeolaceae, are basal to the
Limnanthaceae on the cladogram and are not part of this
subclade. In addition to the families within Brassicales that
we examined, the order contains the following small, often
monogeneric families that have not been examined:
Arabidopsis
Brassica
Cleome
Capparis
Reseda
Gyrostemon
Tovaria
Pentadiplandra
Koeberlinia
Batis
Salvadora
Setchellanthus
Limnanthes
Floerkea
Carica
Moringa
Tropaeolum
Bretschneidera
Akania
Type 3
Type 3
Brassicaceae
Type 3
Type 3
Resedaceae
Gyrostemonaceae
Tovariaceae
Pentadiplandraceae
Koeberliniaceae
Bataceae
Salvadoraceae
Brassicaceae
Type 3
Limnanthaceae
Type 1
Caricaceae
Moringaceae
Type 1
Tropaeolaceae
Bretschneideraceae
Akaniaceae
F I G . 2. Cladogram modi®ed from Rodman et al. (1998) showing the phylogeny of the Brassicales constructed from the nucleotide sequences of
rbcL and 18S nrDNA. Types 1 and 3 refer to the root-epidermal patterning of genera determined in the present study.
Pemberton et al.ÐRoot Epidermal Patterning
Akaniaceae, Bataceae, Bretschneideraceae, Gyrostemonaceae, Koeberliniaceae, Moringaceae, Pentadiplandraceae,
Salvadoraceae and Tovariaceae. From their positions on the
cladogram, we predict that species in the families Bataceae,
Gyrostemonaceae, Koeberliniaceae, Pentadiplandraceae,
Salvadoraceae and Tovariaceae will have Type 3 rootepidermal patterning, whereas species in the other families
will have Type 1 root-epidermal patterning.
One feature shared by all 14 families of the Brassicales
examined to date is the presence of mustard oil glycosides
or glucosinolates (Rodman et al., 1996, 1998). Outside the
Brassicales, these compounds have only been found in the
genus Drypetes (Euphorbiaceae). However, phylogenetic
studies have shown that the Euphorbiaceae is distant from
the Brassicales; it is in the Eurosid I group rather than the
Eurosid II group (Angiosperm Phylogeny Group, 1998).
We found that Drypetes deplanchei and Euphorbia variegata
had Type 1 patterning.
We also found Type 3 patterning in all the species we
examined belonging to the order Caryophyllales sensu lato
except for Mammillaria leucocentra (Cactaceae) (Angiosperm Phylogeny Group, 1998). This order includes the
11 families recognized in the Caryophyllales sensu
stricto (Cronquist, 1988): Achatocarpaceae, Aizoaceae,
Amaranthaceae (including genera previously in the
Chenopodiaceae), Basellaceae, Cactaceae, Caryophyllaceae,
Didiereaceae, Molluginaceae, Nyctaginaceae, Phytolaccaceae and Portulacaceae. It also includes additional families
whose DNA sequence data have recently shown them to be
phylogenetically related to the Caryophyllales sensu stricto
(Nandi et al., 1998): Ancistrocladaceae, Asteropeiaceae,
Dioncophyllaceae, Droseraceae, Frankeniaceae, Nepenthaceae, Plumbaginaceae, Polygonaceae, Rhabdodendraceae,
Simmondsiaceae and Tamaricaceae. For many years, the
families of the Caryophyllales sensu stricto have been
recognized as having a series of morphological and chemical
features unknown in other angiosperms (Cronquist, 1988).
These features include the production of betalains rather
than anthocyanins as ¯ower pigments (except for the
Caryophyllaceae and Molluginaceae) (Mabry, 1976; Cronquist, 1981), and having a characteristic type of sieve-tube
plastid (Behnke, 1981). These families also have ester-linked
ferulic acid in their unligni®ed primary cell walls (Hartley
and Harris, 1981). This character has not been found in any
other dicotyledonous order, but has been found in the
commelinoid monocotyledons (Harris and Hartley, 1980;
Harris, 2000). In addition, many of these families have a
characteristic spherical, pantoporate type of pollen grain
which is rare among other angiosperms (Cronquist, 1988).
The new, enlarged grouping of the Caryophyllales sensu lato
also has a range of features in common, including irregular
secondary growth and an endosperm provided with starch
grains which are not found at high frequencies in other taxa
(Nandi et al., 1998). Type 3 patterning appears to be another
feature that is common in this group. However, it is not
present in the species of Cactaceae (Mammillaria leucocentra) we examined and more families need to be examined.
The Type 3 root-epidermal patterning occurs in three
phylogenetically well separated taxa of eudicotyledons: the
Brassicales (Eurosids II), the Caryophyllales sensu lato
653
(core eudicotyledons outside the Rosids and Asterids), and
the Boraginaceae (Euasterids I). Thus, it appears that this
type of patterning evolved at least three times in the
eudicotyledons. The mechanisms controlling the development of Type 3 root-epidermal patterning in Arabidopsis
thaliana have been studied extensively over the last decade,
with some of the genes involved being characterized and
models proposed for their interactions (Lee and Schiefelbein, 1999; Mendoza and Alvarez-Buylla, 2000). It would
be interesting to determine whether similar genes control
Type 3 root-epidermal patterning in other species of
Brassicaceae and in the other families of Brassicales with
Type 3 root-epidermal patterning. It would be even more
interesting to determine if similar genes control Type 3
root-epidermal patterning in the Caryophyllales sensu lato
and in Nemophila (Boraginaceae) which appear to have
evolved the Type 3 root-epidermal patterning independently of one another and of the Brassicales.
From the present study, root-hair patterning Types 1 and
3 occur in the eudicotyledons, but Type 2 root-hair
patterning either does not occur or is very rare. However,
this type of patterning occurs in the non-eudicotyledons: the
Nymphaeaceae and many monocotyledonous families,
including the Poaceae (Leavitt, 1904; Row and Reeder,
1957). As far as we are aware, Type 3 root-epidermal patterning has not been recorded in angiosperms other than the
eudicotyledons. However, the only major survey of root-hair
patterning which included the non-eudicotyledons (Levitt,
1904) did not recognize Type 3 patterning. Thus, Type 3
root-epidermal patterning may occur in this group of plants.
Clowes (2000) carried out an anatomical examination of
longitudinal and transverse sections of the root apical
meristems of a range of angiosperm species. He examined
these sections for the presence of trichoblasts which he
de®ned as `a cell that is visibly recognizable as the precursor
of a root hair cell'. He recognized two patterns of
trichoblast di€erentiation: in vertical rows resulting from
the unequal division of the mother cell, with the short cell
later becoming the trichoblast; and a radial pattern, seen in
transverse sections, in which trichoblasts arise from
epidermal cells lying on the radii between the radial rows
of cortical cells, with the epidermal cells on the same radii
as the cortical cells not becoming the trichoblasts. These
two patterns of trichoblast di€erentiation would be
expected to result in the formation of Type 2 and 3 rootepidermal patternings, respectively.
Interestingly, Clowes (2000) found that the vertical
pattern of trichoblasts did not occur in the eudicotyledons,
which is consistent with our ®nding no species with Type 2
patterning in this plant group. The vertical pattern of
trichoblasts occurred in many species of monocotyledons,
including the Poaceae, as does the Type 2 root-epidermal
patterning. Furthermore, Clowes (2000) found the radial
pattern of trichoblasts only in eudicotyledons. It occurred
in the same Brassicales families in which we found Type 3
root-epidermal patterning: Brassicaceae (including the
Capparaceae), Resedaceae and Limnanthaceae. It did not
occur in the Tropaeolaceae, a family which has Type 1
root-epidermal patterning. Clowes (2000) also found the
radial pattern of trichoblasts in all the families he examined,
654
Pemberton et al.ÐRoot Epidermal Patterning
except Cactaceae, of the Caryophyllales sensu lato. This is
consistent with our ®nding of Type 3 root-epidermal
patterning in all families we examined in this order, except
for the Cactaceae. Our ®nding of the Type 3 patterning in
Nemophila maculata (Boraginaceae, including Hydrophyllaceae) is also consistent with the ®nding by Clowes (2000)
of the radial pattern of trichoblasts in N. menziesii.
However, Clowes (2000) also found this radial pattern in
the two other species of the Boraginaceae he examined,
whereas the two other species we examined in this family
had Type 1 root-epidermal patterning.
In contrast to our ®ndings on the distribution of the Type
3 patterning, Clowes (2000) found the radial pattern of
trichoblasts in families outside the Brassicales, Caryophyllales sensu lato, and the Boraginaceae (including the
Hydrophyllaceae): the Euphorbiaceae, Salicaceae and Urticaceae in Eurosids I; Onagraceae in Eurosids II; Balsaminaceae and Loasaceae in Asterids; and the Acanthaceae in
Euasterids I (Angiosperm Phylogeny Group, 1998). However, two of the families had species with and species
without trichoblasts: in the Euphorbiaceae, Euphorbia
peplus had them, but Mercurialis perennis did not; in the
Onagraceae, Epilobium parvi¯orum had them, but Circaea
lutetiana did not. Furthermore, in the Urticaceae, Urtica
dioica had trichoblasts, but Clowes (2000) recorded that `a
few roots of Soleirolia (Urticaceae) lack trichoblasts'. Of
these additional families in which Clowes (2000) found the
radial pattern of trichoblasts, we examined taxa in the
Euphorbiaceae, Onagraceae and Balsaminaceae, but, except
for Impatiens, the genera we examined were di€erent to
those examined by Clowes (2000).
Thus, in the Brassicales, the Caryophyllales sensu lato,
and Nemophila maculata (Boraginaceae), it appears that the
presence of the radial pattern of trichoblasts is the precursor
of Type 3 epidermal patterning in seedling roots. However,
we have no evidence that this is the case for the other
families in which the radial pattern of trichoblasts was
found, or indeed for the other two species we examined in
the Boraginaceae. It would be interesting to examine more
species in these other families and to examine both the root
apical meristems for trichoblasts and further back in the
root for the type of patterning of the hair and non-hair cells.
The presence of a radial pattern of trichoblasts as described
by Clowes (2000) does not necessarily preclude subsequent
development into Type 1 epidermal patterning.
AC K N OW L E D G E M E N T S
We thank Dr Ian Hallett, HortResearch Ltd, Auckland for
assistance with scanning electron microscopy.
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