Download Anatomical aspects of angiosperm root evolution

Annals of Botany 112: 223 –238, 2013
doi:10.1093/aob/mcs266, available online at www.aob.oxfordjournals.org
REVIEW: PART OF A SPECIAL ISSUE ON MATCHING ROOTS TO THEIR ENVIRONMENT
Anatomical aspects of angiosperm root evolution
James L. Seago Jr1,* and Danilo D. Fernando2
1
Department of Biological Sciences, SUNY at Oswego, Oswego, NY 13126, USA and 2Department of Environmental
and Forest Biology, SUNY College of Environmental Science and Forestry, Syracuse, NY 13210, USA
* For correspondence. E-mail [email protected]
Received: 29 August 2012 Revision requested: 9 October 2012 Accepted: 9 November 2012 Published electronically: 7 January 2013
† Background and Aims Anatomy had been one of the foundations in our understanding of plant evolutionary
trends and, although recent evo-devo concepts are mostly based on molecular genetics, classical structural information remains useful as ever. Of the various plant organs, the roots have been the least studied, primarily
because of the difficulty in obtaining materials, particularly from large woody species. Therefore, this review
aims to provide an overview of the information that has accumulated on the anatomy of angiosperm roots and
to present possible evolutionary trends between representatives of the major angiosperm clades.
† Scope This review covers an overview of the various aspects of the evolutionary origin of the root. The results
and discussion focus on angiosperm root anatomy and evolution covering representatives from basal angiosperms, magnoliids, monocots and eudicots. We use information from the literature as well as new data from
our own research.
† Key Findings The organization of the root apical meristem (RAM) of Nymphaeales allows for the ground meristem and protoderm to be derived from the same group of initials, similar to those of the monocots, whereas in
Amborellales, magnoliids and eudicots, it is their protoderm and lateral rootcap which are derived from the same
group of initials. Most members of Nymphaeales are similar to monocots in having ephemeral primary roots and
so adventitious roots predominate, whereas Amborellales, Austrobaileyales, magnoliids and eudicots are generally characterized by having primary roots that give rise to a taproot system. Nymphaeales and monocots often
have polyarch (heptarch or more) steles, whereas the rest of the basal angiosperms, magnoliids and eudicots
usually have diarch to hexarch steles.
† Conclusions Angiosperms exhibit highly varied structural patterns in RAM organization; cortex, epidermis and
rootcap origins; and stele patterns. Generally, however, Amborellales, magnoliids and, possibly, Austrobaileyales
are more similar to eudicots, and the Nymphaeales are strongly structurally associated with the monocots, especially the Acorales.
Key words: Anatomy, angiosperms, cortex, epidermis, evolution, roots, vascular tissue.
IN T RO DU C T IO N
Evolutionary origin of the root
A root is a highly differentiated multicellular axis found only
in the sporophytes of vascular plants that typically has a
rootcap, endodermis, pericycle and lateral roots. It is the
main organ in vascular plants that anchors the plant body to
its substrate and absorbs water and dissolved minerals to
support growth and development. The free-living gametophytes of bryophytes, lycophytes and monilophytes grow on
moist environments, and anchorage is accomplished by a
system of unicellular or undifferentiated multicellular rhizoids.
Evolutionarily, the root seemed to be the last of the three main
vegetative organs to evolve, perhaps since early land plants
grew on or near the water and so much of their early innovations were geared toward maximizing photosynthesis through
development of stems and leaves. Vascular plants evolved at
least during the Silurian based on the oldest known macrofossil – Cooksonia (Lang, 1937; Edwards et al., 1992), but
there is no record of specialized root axes in this Period
(Gensel et al., 2001; Raven and Edwards, 2001). In the
Early Devonian, several early land plants already had well
developed stems and leaves, but only structures with considerable similarity to roots are known, such as those of Asteroxylon
mackiei (Rayner, 1984; Li and Edwards, 1995; Gensel et al.,
2001; Bennett and Scheres, 2010). Although no rootcap was
observed from the rooting structures of lycophytes during the
Early Devonian, they had sub-terranean parenchymatous axes
which performed the functions of roots and so these plants
have been considered to have possessed roots (see Raven and
Edwards, 2001). Bennett and Scheres (2010) suggested that
these horizontal axes later evolved rootcap meristems, and so
rootcap formation was a separate innovation that allowed penetrative growth into the soil. There is no corresponding evidence
for root-like structures for the euphyllophytes (monilophytes
and seed plants) during the Early Devonian, and the earliest
convincing evidence of root in this group is from Lorophyton
goense, a Middle Devonian fern-like (cladoxylalean) plant
(Fairon-Demaret and Li, 1993). Roots of extant lycophytes
and euphyllophytes possess a rootcap that is derived from
and functions to protect the root apical meristem (RAM), and
root hairs are present on the epidermis of all major vascular
plants (Jones and Dolan, 2012). Their endodermis ensures a
one-way mode of water transport into the plant, while the pericycle is usually where the lateral roots originate.
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Seago & Fernando — Anatomical aspects of angiosperm root evolution
subtends the embryonic leaf in ferns (Cooke et al., 2004) and,
although the root is formed on the basal pole of the embryo
in angiosperms, it is derived from the hypophysis in eudicots
and ground meristem in monocots (Bennett and Scheres,
2010). All these suggest multiple origins of the roots and therefore warrant further investigations.
It has been hypothesized that roots evolved at least twice,
once in the lycophytes and another in the euphyllophytes
(Bierhorst, 1971; Kenrick and Crane, 1997; Gensel et al.,
2001; Raven and Edwards, 2001; Boyce and Knoll, 2002;
Jones and Dolan, 2012; Pires and Dolan, 2012). Phylogenetic
analysis that integrated key fossil taxa with extant lineages
shows that the roots of lycophytes and euphyllophytes are analogous (Fig. 1) (Friedman et al., 2004). This suggests that the
common ancestors of both lycophytes and euphyllophytes
lack roots, and so the possession of roots must be the result of
exhibiting the same developmental patterns in response to a
similar selective pressure (Friedman et al., 2004). Therefore,
there is strong support for the independent origin of roots in
land plants. However, it is still not clear how many times
roots evolved within the lycophytes and euphyllophytes. In
plants with pyramidal root apical cells [e.g. monilophytes and
some lycophytes (Selaginella)], lateral roots arise from the
endodermis, whereas in plants with one or more superimposed
initials [e.g. seed plants and some lycophytes (Lycopodium)],
lateral roots originate from the pericycle. The orientation and
origin of the embryonic root axis relative to the shoot axis are
different in monilophytes and seed plants (Gensel et al., 2001;
Raven and Edwards, 2001). Specifically, the embryonic root
Developmental origin of the root
The early vascular plants were composed of dichotomously
branched parenchymatous axes or telomes based from the
Rhynie Chert fossils. In the Zosterophyllophyta of the Early
Devonian, most of the branches were erect and functioned as
the main organ for photosynthesis (shoot-like), whereas other
branches were oriented horizontally and rested on the surface
of the substrate. Some of the horizontal axes were directed
downwards and were root-like in appearance. Based on this,
the roots of extant lycophytes and euphyllophytes probably
arose from an original dichotomizing axis, particularly from
the horizontal branches that penetrated the substrate, anchored
the plant body, and absorbed water and dissolved minerals.
Thus, roots and shoots are considered homologous since
they are both believed to have evolved from the same
Embryophytes
Polysporangiophytes
Tracheophytes
Euphyllophytes
Lycophytes
Lignophytes
Gnetales
Ginkgoales
Conifers
Cycadales
Angiosperms
Archaeopteridales
Seed plants
Elkinsia
Aneurophytales
Ophioglossales
Marattiales
Psilotales
Psilophyton
Isoetales
Lycopodiales
Selaginellales
Rhyniopsida
Zosterophyllum
Aglaophyton
Hornworts
Mosses
Complex thalloid
Haplomitriales
Jungenmanniales
Simple thalloid
Charales
Lycopsida
Sphenophyta
Moniliformopses
Filicales
Liverworts
Roots
Absent
Root-like structure
Roots
F I G . 1. Key fossil taxa are integrated into a phylogeny for analysis of root evolution which shows two evolutionary origins of roots. One origin is in the lycopsida, perhaps from telomic systems that grow into substrate, as found in the Zosterophyllum. Another independent origin is observed in the common ancestor
of extant euphyllophytes. Illustration from Friedman et al. (2004, p. 1728), with permission from the American Journal of Botany.
Seago & Fernando — Anatomical aspects of angiosperm root evolution
dichotomously branched axes (Gensel et al., 2001; Friedman,
2004; Bennett and Scheres, 2010).
Molecular, developmental and genetic analyses are congruent with the fact that, at least in angiosperms, roots and shoots
are derived from the same dichotomizing axes (Friedman,
2004). In Arabidopsis thaliana, these two organs share many
developmental processes in common such as the: (1) formation
of the endodermis which both require the expression of
SCARECROW and SHORTROOT genes (Pysh et al., 1999;
Nakajima et al., 2001); (2) regulation of radial patterning of
the ground tissues during and post-embryo formation (Fukaki
et al., 1998; Wysocka-Diller et al., 2000); (3) specification
of epidermal cell fate, e.g. GLABRA2 in conjunction with
WEREWOLF genes (in roots) and its functionally redundant
paralogue GLABRA1 (in shoots) are required for the differentiation between hair- and non-hair-bearing cells in roots and
shoots (Dolan and Scheres, 1998; Schiefelbein, 2003; Bruex
et al., 2012); (4) provascular cell fate commitment
(Scarpella et al., 2000); and (5) similar mutations affecting
both the RAM and the shoot apical meristem (SAM) (Ueda
et al., 2004).
It is becoming clear that the production and maintenance of
stem cells in the RAM and SAM involve the same developmental patterns (Mayer et al., 1998; Haecker et al., 2004)
and expression of the same genes or class of genes including
SCARECROW (Wysocka-Diller et al., 2000), WUSCHEL
RELATED HOMEOBOX (Haecker et al., 2004), HALTED
ROOT (Ueda et al., 2004) and the CLAVATA3/ENDOSPERM
SURROUNDING REGION-related gene family (Miwa et al.,
2009). The stem cells in the RAM and SAM are located in
regions referred to as the quiescent centre and organizing
centre, respectively, which are the signalling centres that
make up the stem cell maintaining microenvironments in
both meristems. These two regions are considered to be functionally equivalent (Baurle and Laux, 2003; Byrne et al.,
2003; Haecker et al., 2004; Veit, 2004; Bennett and Scheres,
2010). There are many similarities in the organizations of
the RAM and SAM, and the signalling components required
for stem cell initiation and maintenance seem to be relatively
conserved. This suggests that similar genes or classes of
genes have been co-opted for use in both types of meristems
(Friedman et al., 2004; Bennett and Scheres, 2010). Bennett
and Scheres (2010) have proposed a mechanism for how the
RAM and SAM of monilophytes and seed plants descended
from the ancestral generic meristem of a dichotomizing axis.
Origin of genes involved in root development
The genome sequence of the model bryophyte
Physcomitrella patens has provided the opportunity to probe
the genes, gene expression patterns and development associated with the gametophyte phase of the plant life cycle. It
also has allowed for the comparison of sequences and analysis
of evolutionary trends across phyla and between the gametophyte and sporophyte generations of the plant life cycle.
Molecular genetic analysis of root and shoot development
does not only suggests homology of roots and shoots, but
also that genes involved in the formation of gametophyterelated structures in ancestral plants were co-opted to
perform regulatory roles in the formation of sporophyte-related
225
structures in more evolutionarily derived plants. This is exemplified by the ROOT HAIR DEFECTIVE 6 (RHD6) and
RHD6-LIKE 1 (RSL1) genes that control the differentiation
of roots hairs in A. thaliana, and two similar genes (PpRSL1
and PpRSL2) that are involved in rhizoid development in
P. patens (Menand et al., 2007). Rhizoids and root hairs
both elongate by tip growth and fulfil similar functions
(Jones and Dolan, 2012). However, rhizoids are gametophytic
filamentous structures from the gametophytes, whereas root
hairs are sporophytic tubular projections from root epidermis.
It appears that genes that promoted the development of cells
with rooting functions in the gametophytes of bryophytes
were co-opted in the development of the sporophytes of vascular plants or their ancestors, perhaps through gene duplication
and sub-functualization. Once expressed in the sporophyte,
they promoted the development of hairs on roots. It is also possible that changes in the cis-regulatory regions of RSL1 genes
played a role in altering their expression patterns, i.e. promotion of their transcription in the sporophytes and repression
of their transcription in the gametophytes (Jones and Dolan,
2012). The elaboration of the sporophyte generation of the vascular plants and particularly the large radiation of morphological forms that occurred during the Devonian may have
been achieved in part through the recruitment of genes or
genetic networks that had previously evolved and functioned
in the gametophyte generation of early land plants or their
ancestors. The demonstration that similar genes control the development of cells with a rooting function suggests that gene
recruitment is an ancient mechanism (Edwards and Feehan,
1980; Menand et al., 2007). Therefore, RHD6 and RSL1
genes control the development of cells with rooting functions
in bryophytes and angiosperms. However, it remains to be seen
if these genes will exhibit the same function in lycophytes,
monilophytes and gymnosperms. Also, it is likely that there
are other genes involved in the development of roots and
other structures in the sporophyte that were recruited from
the gametophyte. Therefore, investigations into the molecular
genetics of root structure and development in basal land
plants will address the questions regarding homology of
roots and shoots and multiple origins of the roots. Our understanding of the diversity of root anatomical structures will also
help in formulating or substantiating possible evolutionary
relationships.
Angiosperm root anatomy and evolution
Much work has been done on the anatomy and development
of roots of extant angiosperms, particularly from model herbaceous species such as A. thaliana and Oryza sativa, and other
species of economic importance such as Zea mays and Glycine
max, plants that are considered to be more evolutionarily
derived. To bridge the gap in our understanding of root structures, development and evolution, a review of our knowledge
of this subject that includes the major clades of the angiosperms is necessary. Therefore, this article will cover root structures from plants representing the basal angiosperm lineages,
such as Amborellales, Nymphaeales and Austrobaileyales
(Heimsch and Seago, 2008), and representative magnoliids,
monocots and eudicots. Data will be derived from the literature, including our articles, and from some new research,
226
Seago & Fernando — Anatomical aspects of angiosperm root evolution
with methods, including brightfield and epifluorescence photomicroscopy, from Seago et al. (1999b, 2005), Seago (2002),
Soukup et al. (2005) and Heimsch and Seago (2008).
Formation of below-ground axes from rhizomes into roots
has been considered with regard to various ecological and
functional aspects of evolutionary phenomena (e.g. Cairney,
2000; Raven and Edwards, 2001; Brundrett, 2002; Sperry,
2003; Jackson et al., 2009; Pires and Dolan, 2012).
However, more generally with regard to angiosperms,
researchers have examined structural features such as the transition from tracheids to vessel elements and specific xylem
cells associated with water/mineral conduction (Carlquist,
1975; Carlquist and Schneider, 2001, 2002, 2009; Schneider
and Carlquist, 2002), RAMs (Philipson, 1990; Barlow, 1994,
2002; Clowes, 2000; Groot and Rost, 2001; Groot et al.,
2004; Heimsch and Seago, 2008) and, to a lesser degree, the
cortical derivatives of the RAM (Shishkoff, 1987; Seago
et al., 2005).
There are generally two very different developmental and
structural aspects to angiosperm root systems. The primary
root system is derived from the radicle and tends to be dominant in eudicots, and gives rise to lateral roots with various
degrees of branching. In monocots, the primary root is often
ephemeral, and so adventitious roots (derived usually from
stems and leaves) and seminal roots (derived from mesocotyl)
comprise their root systems where they also produce lateral
roots (Bell and Bryan, 2008, p. 126; for nature of seminal
roots, cf. Weaver, 1926; Hayward, 1938). The ephemeral
nature of primary roots and dominance of adventitious roots
in monocots present a difficulty in comparisons, especially
since adventitious roots (even from secondary growth) also
occur in many eudicots. However, it seems quite likely that
at least some groups of basal angiosperms were derived from
ancestors whose plant structure was mainly rhizomatous
prior to flower evolution. Nevertheless, besides the difference
in the origin of primary and adventitious roots, there is generally no difference in the anatomy of primary and adventitious
roots, primary roots and their lateral roots, and adventitious
roots and their lateral roots in angiosperms. However, as will
be realized in this review, the differences lie in the types or
groups of plants and their environments.
DATA FROM TH E L ITE RAT U RE
AN D NE W R E SU LT S
Amborellales
This order is represented by Amborella trichopoda, the only
member of the family Amborellaceae. It is an understorey
shrub or small tree on moist soils or near streams, and is
endemic to New Caledonia. Adventitious and lateral roots
are characterized by a diarch stele, but triarch steles are also
present; secondary xylem has tracheids but no vessels
(Carlquist and Schneider, 2001). The cortex is delimited to
the inside by an endodermis with distinct Casparian bands
(CBs) and suberin lamellae (SL; Fig. 2A, B) with passage
cells (Fig. 2C). The middle cortex is occupied by non-radially
arranged parenchyma cells (Fig. 2B – D; Heimsch and Seago,
2008), and there is no aerenchyma. Secondary xylem is accompanied by more cells of the endodermis developing SL
(cf. Fig. 2A – C); endodermal cells dilatate or increase in
number as some cells of the adjacent cortex layer thicken
through addition of wall material that is fluorescent (cf.
Fig. 2C, D), but the endodermis does not undergo this kind
of dilatation as in some eudicots (Lux and Luxová, 2003;
Šottnı́ková and Lux, 2003). An irregular, multilayered hypodermis with an exodermis with CBs and SL underlies the epidermis (Fig. 2B– D). Both endodermis and exodermis remain
before pericyclic derivatives initiate periderm production.
Amborella RAMs are eudicot-like (Heimsch and Seago, 2008).
Nymphaeales
The Nymphaeales are currently and historically aquatic (Les
and Schneider, 1995; Friis et al., 1999, 2001, 2009). Roots of
Nymphaeaceae and Cabombaceae are always adventitious in
water and have been previously characterized (Seago, 2002;
Seago et al., 2000b, 2005; Carlquist and Schneider, 2002,
2009). The salient traits are pentarch to polyarch stele in
Nymphaeaceae (Fig. 3D, E) and often monarch stele in the extremely small roots of the Cabombaceae (Fig. 3C, two xylem
cells) and Hydatellaceae (Fig. 3A; cf. Arabidopsis of eudicots,
Baum et al., 2002). However, Conard (1905) described diarchy
in Nymphaea species, but such a condition has not been confirmed because of the ephemeral nature of the primary roots.
Distinctive expansigenous aerenchyma is present in the
Nymphaeaceae and Cabombaceae. An endodermis with CBs
and sometimes a small amount of SL, prominent astrosclereids
of the Nymphaeaceae and their absence in other Nymphaeales,
and uniseriate exodermis with CBs and SL (Fig. 3D, E; Seago
et al., 2005) are also salient features of the Nymphaeales.
Trithuria filamentosa, a representative of the family
Hydatellaceae, usually has one central tracheid surrounded
by phloem (Fig. 3A) and pericycle (our results; Rudall et al.,
2007), but we have also observed two tracheids in the stele;
xylem of T. filamentosa lacks vessels, unlike the
Nymphaeaceae and Cabombaceae (Carlquist and Schneider,
2009). We show here clearly that T. filamentosa has a cortex
with an endodermis with CBs in anticlinal walls, and, like
Cabomba, the SL are more prominent on the outer tangential
walls (note: root endodermis is continuous with the stem endodermis). In the Hydatellaceae, the cortical aerenchyma is
derived through schizogeny, followed by expansigeny
(Fig. 3B, right insert). There is an exodermis with CBs and
SL under the epidermis (Fig. 3A).
A brief depiction of the RAM and root tip of T. filamentosa
is necessary; there is a closed, three-tiered meristem with a distinct, distal tier for the very small rootcap, a separate tier of
ground meristem/protoderm for cortex and epidermis, and
the proximal tier is for the procambium (Fig. 3B; Heimsch
and Seago, 2008). Its RAM appears slightly more monocot
like (tiered monocot in Heimsch and Seago, 2008) than
Cabomba-like (tiered basal angiosperm in Heimsch and
Seago, 2008). The root tip of T. filamentosa does not have a
cleft separating the lateral rootcap from the epidermis, and
the rootcap and its portion of the RAM overlie the protoderm/ground meristem tier (Fig. 3B). This is very similar to
the closed or tiered RAM of the monocots under the
Heimsch and Seago (2008) characterization (and also
Clowes, 2000). In T. filamentosa, the tier for ground
Seago & Fernando — Anatomical aspects of angiosperm root evolution
A
B
227
C
D
E
F
F I G . 2. Basal angiosperms, Amborellaceae and Austrobaileyales: Amborella trichopoda (A) Diarch. Early exodermis. Scale bar ¼ 110 mm. (B) Diarch with
xylem continuous across poles, endodermis with early suberin lamellae (SL) development. Complex exodermis. Mid-cortex non-radial. Scale bar ¼ 120 mm.
(C) Secondary growth, endodermis with SL and passage cells. Scale bar ¼ 120 mm. (D) Redivided endodermis, and some evidence of redivided mid-cortex
and exodermis cells; secondary xylem without vessels, phloem surrounding secondary xylem. Scale bar ¼ 80 mm. Illicium floridanum (E) Diarch root with
Casparian bands and early suberin formation. Scale bar ¼ 140 mm. (F) Secondary xylem with vessels and redivided endodermis with SL, and some evidence
of redivided exodermal cells. Scale bar ¼ 130 mm. Abbreviations (used both here and on other figures): c, cortex; e, epidermis; en, endodermis; ex, exodermis,
l, lacuna; p, passage cell of endodermis; s, secondary xylem; v, velamen; x, primary xylem.
meristem/protoderm is most clearly aligned with the epidermis, and there is a very clear distinction between the rootcap
initials and the ground meristem/protoderm. The images of
newly germinated T. submersa primary roots in Rudall et al.
(2009) and in Friedman et al. (2012; their fig. 6A) appear to
be very similar to our image in Fig. 3B. Further, Fig 3B
(left insert) shows a radial arrangement of cortical cell files
that are like monocots derived from tiered monocot RAMs
(Heimsch and Seago, 2008); this distinctive radial cortex is
not usually found in the Cabombaceae (Seago, 2002; Seago
et al., 2005; Heimsch and Seago, 2008). Strangely, the RAM
and root tip of some Lemnaceae (Araceae, Alismatales) are
very similar to the Cabomba-tiered basal angiosperm-type
RAM with a cleft between the lateral rootcap and epidermis
(see Landolt, 1998), except that its RAM has more pronounced
tiered monocot cell lineages like Trithuria.
Austrobaileyales
Illicium floridanum is used here as a representative of the
order. Like other members of this clade, it is terrestrial
(Thomas, 1914; Metcalfe, 1987); its lateral roots are often
small and diarch, with early-maturing phloem fibres and an
endodermis with CBs and SL delimiting a very small cortex
with some radial cell patterns and without an exodermis
(Fig. 2E). Its adventitious roots are mostly diarch (Metcalfe,
1987), but tetrarch patterns are also found, and early secondary
growth produces secondary xylem with vessel elements, a
narrow phloem region without noticeable pericyclic development into phellogen, and a redivided endodermis, fully complete with CBs and even thick SL (Fig. 2F); and an
extensive hypodermis which is probably exodermal. These
roots show a much more extensive cortex with irregular cell
patterns, typical of an open RAM origin for cortex, although
228
Seago & Fernando — Anatomical aspects of angiosperm root evolution
A
C
D
B
E
F I G . 3. Basal angiosperms, Nymphaeales: (A) Trithuria filamentosa – monarch stele, nine-celled endodermis with Casparian bands (CBs) and suberin lamellae
(SL), mid-cortex with aerenchyma and collapsed radiating cells, exodermis and epidermis. Scale bar ¼ 20 mm. (B) Median longisection of root tip with tiered
basal angiosperm (TB) apical organization (arrow). Scale bar ¼ 20 mm. Insets: left – radial cortical cell files, scale bar ¼ 40 mm; right – aerenchyma lacunae
expanded by cell expansion, scale bar ¼ 35 mm. (C) Cabomba caroliniana – monarch stele, nine-celled endodermis, schizogenous– expansigenous aerenchyma,
exodermis with double CBs; photograph from Seago (2002), with permission from the Journal of the Torrey Botanical Society. Scale bar ¼ 65 mm. (D) Nuphar
lutea – polyarch stele, astrosclereids in expansigenous aerenchyma, exodermis with CBs and SL; photograph from Seago (2002), with permission from the Torrey
Botanical Society. Scale bar ¼ 200 mm. (E) Nymphaea odorata – polyarch stele (seven xylem poles), astrosclereids, expansigenous aerenchyma. Scale bar ¼
60 mm. See Fig. 2 for list of abbreviations.
lateral roots have monocot-like RAMs (Heimsch and Seago,
2008).
Magnoliids
This clade is represented by four orders, i.e. Canellales,
Laurales, Magnoliales and Piperales (APG, 2009). However,
since there is no information on the roots of the Canellales, we
will deal only with the representative families from the other
three orders: Calycanthaceae, Lauraceae, Magnoliaceae,
Annonaceae, Aristolochiaceae, Piperaceae and Saururaceae.
The magnoliids are terrestrial and their primary and lateral
roots vary from diarch to hexarch ( present study; Thomas,
1914; Metcalfe and Chalk, 1950a, b; Metcalfe, 1987); they are
Seago & Fernando — Anatomical aspects of angiosperm root evolution
usually tetrarch or pentarch, but hexarch is also common (e.g.
Magnolia, Liriodendron, Asimina, Laurus, Aristolochia,
Saururus; Fig. 4A– D). For primary roots, Calycanthus and
Asimina (see Thomas, 1914; Hayat and Canright, 1965;
Metcalfe, 1987) are initially diarch and Saururus is tetrarch
( present study; Calycanthus may also be tetrarch, Thomas,
1914). Adventitious and lateral roots in Laurus (Lauraceae)
and Aristolochia (Aristolochiaceae) can also be tetrarch or
diarch (with two distinct and widely separate protophloem elements at each pole). In the Piperaceae, Metcalfe (1987) reported
diarchy and tetrarchy in Peperomia and polyarchy in Piper. In
most magnoliids, the centre of the stele often is occupied by
metaxylem (Fig. 4B, C) or sclerenchyma (Fig. 4D). A pericycle
delimits the stele, and the cortex is delimited on its interior by an
229
endodermis which forms CBs and later SL; there is usually a uniseriate exodermis (Fig. 4B, D); depending on the state of early
secondary growth, an epidermis may or may not be present in
older roots after exodermis maturation. Endodermis and exodermis increase in cell number during secondary growth. All magnoliids so far reported have common initials in their RAMs
(Heimsch and Seago, 2008).
Monocots
Most monocot roots are adventitious and arise endogenously
usually from stems or leaves (Tomlinson, 1961, 1969, 1982;
Metcalfe, 1971; Ayensu, 1972; Keating, 2002; Bell and
Bryan, 2008). In mature roots, the stele is often polyarch (six
A
B
C
D
F I G . 4. Magnoliids, Magnoliales. (A) Magnolia soulangeana – young root, hexarch stele, endodermis. Scale bar ¼ 65 mm. (B) Secondary xylem with vessels,
redivided endodermis with suberin lamellae (SL) and passage cells, exodermis. Scale bar ¼ 30 mm. (C) Aristolochia sp. – tetrarch stele with early secondary
xylem, endodermis with Casparian bands (CBs) and early suberin deposition, early stage of exodermis wall deposition. Scale bar ¼ 55 mm. (D) Saururus
cernuus – tetrarch root with early secondary growth, endodermal CBs, exodermis with CBs and partial SL. Scale bar ¼ 115 mm. See Fig. 2 for list of
abbreviations.
230
Seago & Fernando — Anatomical aspects of angiosperm root evolution
A
B
C
D
E
F
I
G
J
H
K
F I G . 5. Monocots. (A) Acorus calamus – root from epidermis, exodermis, expansigenous aerenchyma, endodermis and polyarch stele with sclerenchyma pith; photograph from Seago et al. (2005). Scale bar ¼ 190 mm, (B) Leucojum aestivum – exodermis with passage cells, endodermis with Casparian bands (CBs) and suberin
lamellae (SL) opposite multiple phloem poles. Scale bar ¼ 190 mm. (C) Iris pseudacorus – polyarch stele with xylem cells embedded in sclerenchyma through a pith,
narrow endodermis cells with distinctive secondary thickenings, mid-cortex with some lysigenous cavities, thick-walled exodermis, epidermis, photograph courtesy of
Chris Meyer. (D) Typha glauca – multiseriate exodermis and uniseriate endodermis with CBs, SL and secondary lignified walls, mostly schizogenous aerenchyma,
polyarch stele, sclerenchymatous pith; photograph from Seago et al. (2005). Scale bar ¼ 300 mm. (E) Eichhornia crassipes – multiseriate hypodermis but biseriate
exodermis, distorted mid-cortex (actually expansigenous/lysigenous), inner cortex cells with cellulose thickenings, polyarch stele (often 16+ xylem and phloem poles),
pith. Scale bar ¼ 75 mm. (F) Pandanus utilis – aerial root, polyarch stele (often 20–40 poles) with sclerenchyma bundles scattered throughout parenchyma in stele and
cortex, biseriate exodermis and uniseriate endodermis with secondary lignified walls. (G) Zea mays – polyarch stele, endodermis with suberin lamellae, thick-walled
epidermis and young exodermis; photograph courtesy of Chris Meyer. (H) Dendrobium sp. – multiple epidermis or velamen, uniseriate exodermiswith lignified secondary wall, tears in cortical tissue, endodermis with suberin lamellae and passage cells, polyarch stele and scattered fibres in pith. Scale bar ¼ 60 mm. (I) Hydrocharis
morsus-ranae – triarch stele with lysigenous aerenchyma and cellulose-thickened cortex layer next to endodermis, no exodermis. Scale bar ¼ 150 mm. (J) Zingiber
officinale – polyarch stele with central parenchymatous pith surrounded by sclerenchyma, endodermis and exodermis uniseriate with secondarily lignified walls.
(K) Allium cepa – face-view of exodermis with long cells and short cells (arrows), autofluorescence of CBs and SL in violet light; photograph courtesy of Daryl
Enstone. Scale bar ¼ 85 mm. See Fig. 2 for list of abbreviations.
or more poles of xylem and phloem; Fig. 5A –H, J), but three
xylem and phloem strands can be found, especially in wetland
or aquatic plant roots such as Hydrocharis (Fig. 5I; Seago
et al., 1999a). Tomlinson (1982) noted reduced numbers of
poles for plants with floating roots in the Alismatales. Even
Acorus, usually reported with six to nine poles of xylem and
Seago & Fernando — Anatomical aspects of angiosperm root evolution
phloem (Keating, 2002; Soukup et al., 2005), may have only
five poles (Soukup et al., 2005). Very high numbers of
strands (≥20) occur in plants with large and/or aerial roots
such as in Pandanaceae and Arecaceae (Fig. 5F, G, J;
Tomlinson, 1961, 1982; French, 1987a, b).
Figure 5 shows other features of some diverse monocots
from the Acorales to the Zingiberales. The endodermis is uniseriate and most often has cell wall stages I, II and III [e.g.
Fig. 5C, D, F, H, J; see Meyer et al. (2009) for endodermal
cell wall stages]. The middle cortex has great variability, but
one of the most unique features is the occurrence of sclerenchyma bundles in roots of many aerial plants (Fig. 5F;
Tomlinson, 1961; Keating, 2002). Aerenchyma is a common
feature in the many families with aquatic or wetland species
(Fig. 5A, B, D). In basal monocots (Acorus), aerenchyma is
expansigenous, and in derived monocots it is often of
varying schizo-lysigenous to lysigenous types (Fig. 5I; Seago
et al., 2005; Jung et al., 2008). However, aerenchyma patterns
in most angiosperms are still not well represented (Jackson
et al., 2009; Van der Valk, 2012), except that the members
of Cyperaceae are well known for their unusual tangential lysigeny (Seago et al., 2005; see also Metcalfe, 1971). Often, in
plants with aerial roots, especially large roots, the air spaces
in the cortex are described as cavities (Tomlinson, 1961)
because they are not developed or organized like typical aerenchyma. A hypodermis ranges from uniseriate to multiseriate exodermis (Fig. 5A, C – H, J), and in many plants is
dimorphic with long and short cells (Fig. 5K; Shishkoff,
1987). A velamen occurs in some aerial roots, especially in
orchids (Fig. 5H; Ayensu, 1962; Zankowski, 1987; Keating,
2002).
The single most distinctive feature of monocots, as reported
extensively by Clowes (2000) and Heimsch and Seago (2008),
is the developmental association between ground meristem and
protoderm in the RAM.
Eudicots
As early as 1914, Thomas compared the vasculature of
many seedling roots that are now classified as either magnoliids or eudicots; he found them to vary from diarch to
octarch, but in Metcalfe and Chalk (1950a, b) and Metcalfe
(1987) very few species’ roots are heptarch and octarch. In
the basal eudicot Ranunculales, there is diarchy (Aquilegia,
some Ranunculus; Thomas, 1914), tetrarchy (other
Ranunculus, Berberis; Thomas, 1914) and pentarchy
(Podophyllum). Thus, while vascular tissues of the stele in
most eudicots have two to six poles or strands of alternating
xylem and phloem (Fig. 6A, E – I; Metcalfe and Chalk,
1950a, b), importantly, some groups near the base of the eudicots (Proteales) and core eudicots (Gunnerales) often have
polyarch steles. Nelumbo lutea (Proteales, Nelumbonaceae;
Fig. 6B) is aquatic, but Gunnera (Gunnerales, Gunneraceae)
grows both in aquatic and terrestrial habitats, and its species
often have large differences in numbers of xylem poles even
in terrestrial plants, as we have collected (cf. G. perpensa,
Fig. 6C, and G. killipiana, Fig. 6D), even though the roots
may be similar or dissimilar in size; tetrarch steles are apparently characteristic of these basal species (J.L. Seago, pers.
obs.; A. Soukup and E. Tylová, pers. comm.; Wilkinson,
231
2000). Roots of species across the eudicot spectrum may
have diarchy (Fig. 6I; e.g. Thomas, 1914; Hayward, 1938;
Baum et al., 2002), especially when those roots are small, as
in secondary root stages (Seago, 1973; Byrne et al., 1977).
In many Fabaceae, primary roots are often triarch to hexarch
(Fig. 6E), although in Glycine lateral roots originate in the
diarch condition (Ambler et al., 1971) and then develop tetrarchy (Byrne et al., 1977); tetrarchy is very common in eudicots (Metcalfe and Chalk, 1950a, b; Seago, 1971).
The cortex is delimited internally by the endodermis which
varies as much in eudicots as it does in monocots, and often
passage cells with CBs are opposite protoxylem and SL cells
are opposite the protophloem (Fig. 6A, B, G); stage III cell
walls appear to be less common in eudicots. Air spaces in the
form of aerenchyma are found most commonly in aquatic eudicots (e.g. Fig. 6G, H). There is an exodermis in many eudicots
(e.g. Fig. 6A–C, H), but it is typically lacking in noduleproducing roots with an open transversal RAM such as
legumes (Heimsch and Seago, 2008). Many eudicots, especially
the many trees and shrubs, have secondary root growth, even if
very limited as in small herbaceous plants (e.g. Fig. 6F;
Metcalfe and Chalk, 1950a, b). Secondary root growth is probably accompanied by a dilatated endodermis and exodermis in
many species, as in Gentiana (Fig. 6J; Šottniková and Lux,
2003) and Medicago (our observations).
Resin canals in roots are known but relatively little studied
(French, 1987a). Laticifers are more a feature of eudicots (e.g.
Ipomoea purpurea; Seago, 1971; and Lactuca sativa, J.L.
Seago, pers. obs.; see also Metcalfe and Chalk, 1950a, b;
Metcalfe, 1967) than of monocots where they are rare
(Metcalf, 1967). Root laticifer development has been studied
(e.g. Seago, 1971), and crystalliferous and tanniniferous cells, especially in rootcap or cortex, are also well known (e.g. Seago and
Marsh, 1989).
All eudicots have a RAM with the protoderm/epidermis
associated developmentally with the lateral rootcap (Clowes,
2000; Groot et al., 2004; Heimsch and Seago, 2008).
Air spaces in roots
Aerenchyma types have been presented by several researchers (e.g. Justin and Armstrong, 1987; Evans, 2004), but the
explanations for the development of intercellular spaces into
aerenchymatous lacunae by Seago et al. (2005) are the only
adequate explanations for the roles of cell division, cell expansion, cell separations and cell deaths that can account for the
types of root cortical aerenchyma: expansigeny, schizogeny
and lysigeny. Based on this feature, Seago et al. (2005) and
Jung et al. (2008) best provide the possible evolutionary
path from basal angiosperms to monocots or eudicots.
Clearly, the earliest root aerenchyma in angiosperms was
most probably by expansigeny (Fig. 7A – Acorus;
Nymphaeales of basal angiosperms and Acorales of monocots;
Seago et al., 2005; Soukup et al., 2005), the lacunae arising by
cell division and cell expansion, not by schizogeny (Fig. 7B)
or lysigeny (Fig. 7C, as noted by Jackson et al., 2009).
Particularly in monocots, various kinds of lysigeny arose in
more derived families of several orders. The occurrence of diaphragms across aerenchymatous lacunae has been noted
and even studied in detail (e.g. in Cabombaceae and
232
Seago & Fernando — Anatomical aspects of angiosperm root evolution
A
B
C
D
E
F
G
H
I
J
F I G . 6. Eudicots. (A) Ranunculus repens – tetrarch stele, endodermis with passage cells, cortex non-aligned, exodermis Casparian bands (CBs) and suberin
lamellae (SL); brightly fluorescing epidermis. Scale bar ¼ 85 mm. (B) Nelumbo lutea – polyarch stele with sclerified pith, endodermis with passage cells
and suberized cells, exodermis suberized. Scale bar ¼ 115 mm. (C) Gunnera perpensa – polyarch stele (seven poles), endodermis, mid-cortex with expansigenous spaces, endodermis with CBs and SL. Scale bar ¼ 190 mm. (D) Gunnera killipiana – polyarch stele with 18 xylem strands, bundles within pith and parenchyma. Scale bar ¼ 200 mm. (E) Medicago sativa – typical legume triarch stele, non-radial cortex, no hypodermis/exodermis. Scale bar ¼ 95 mm; inset:
somewhat unusual tetrarch stele observed in very few primary roots. (F) Fraxinus americana – secondary xylem, but pentarch primary xylem visible. Scale
bar ¼ 140 mm. (G) Rumex crispus – pentarch stele with partial sixth pole and central metaxylem, endodermis with CBs, expansigenous aerenchyma, no exodermis. Scale bar ¼ 135 mm. (H) Nymphoides crenata – pentarch with pith, endodermis with CBs only and exodermis with CBs and SL, astrosclereids in midcortex with aerenchyma. (I) Artemisia lavandulaefolia – diarch primary root, no pith, endodermis with CBs only, faint CB staining in hypodermis; photograph
courtesy of Chaodong Yang. Scale bar ¼ 80 mm. (J) Gentiana asclepiadea – root with dilatated endodermis and exodermis in early secondary growth; photograph courtesy of Alexander Lux. Scale bar ¼ 45 mm. See Fig. 2 for list of abbreviations.
Seago & Fernando — Anatomical aspects of angiosperm root evolution
A
B
C
233
D
F I G . 7. Aerenchyma, air cavities. (A) Expansigeny – cell division and cell expansion, in Acorus calamus; photograph courtesy of Aleš Soukup. Scale bar ¼
60 mm. (B) Schizogeny – cell wall separations, in Typha glauca; photograph from Seago et al. (2005). Scale bar ¼ 90 mm. (C) Lysigeny – cell deaths, in Oryza
sativa; photograph courtesy of Aleš Soukup. Scale bar ¼ 140 mm. (D) Vascular or stelar air cavity (asterisk) – cell/tissue death, in Pisum sativum; photograph
courtesy of Daniel Gladish and Suma Sreekanta. Scale bar ¼ 150 mm. See Fig. 2 for list of abbreviations.
Nymphaeaceae of the Nymphaeales, Seago et al., 2005; the
Hydatellaceae do not appear to have diaphragms, possibly a
consequence of having only cell expansion and no further
cell divisions contributing to the lacunae). The presence or
absence of diaphragms has not been widely studied across
monocots and eudicots (Seago et al., 2005).
In legumes, vascular cavities can be found in the pith of
some triarch Pisum roots (Fig. 7D) under flooded conditions
(Niki and Gladish, 2001). Legumes do not have the cortex development or structures that allow easy formation of aerenchyma (Seago et al., 2005) or exodermis (Heimsch and
Seago, 2008). Such cavities are not considered aerenchyma.
Secondary aerenchyma, aerenchymatous phellem derived
from phellogen, can also occur in wetland plants (Lythrum salicaria; Stevens et al., 1997) and may be found in the fossil
record in related species (see Little and Stockey, 2003).
DISCUSSION ON SELECTED ASPECTS
OF ROOT A NATOMY
cortex, because such a type of anatomy is not found in
Amborellaceae, magnoliids and eudicots. These patterns
clearly arose in the ancestors of monocots, i.e. various ancestral, early basal angiosperms, as the patterns of epidermis and
lateral rootcap connections characteristic of some basal angiosperms and all eudicots must have separately so arisen.
Further, there appears to be a clear association between
RAM organization and the patterns of lateral rootcap cells
and their sloughing (Hamamoto et al., 2006). Open RAM produces more cells and releases individual living border cells,
whereas closed RAM releases sheets or groups of dead cells.
The fate of lateral rootcap cells in the tiered or closed RAMs
of Cabombaceae and Hydatellaceae, as well as the open transversal RAMs of Nymphaeaceae, need to be examined to determine if the same relationships holds for RAMs of these basal
angiosperms. The differentiation of epidermal cells, especially
in simple tiered RAMs, has received enormous attention in just
a select few species (Bruex et al., 2012; Jones and Dolan,
2012), and this needs to be expanded.
Root apical meristem
Cortex: endodermis and hypodermis
From the concepts of Barlow (1994, 2002) on increasing complexity and quiescence, to Clowes (1994) on epidermis origins,
the possible evolutionary path of RAM organization has been
presented in three major studies by Clowes (2000), Groot et al.
(2004) and Heimsch and Seago (2008). The latter authors presented an analysis of RAMs with several manifestations of
closed and open types and reported that some specimens of
Amborella trichopoda and the magnoliids contain common
initials for most meristematic tissues of the root. As stated
above, Heimsch and Seago (2008) further related the open
and closed RAMs (with cortex and epidermis association) in
the nymphaealean families (Cabombaceae, Nymphaeaceae
and now the Hydatellaceae) to the monocots. In Friedman
et al. (2012), fig. 6 corroborates our findings herein for
T. filamentosa that its primary, adventitious and lateral roots
have a tiered monocot-type RAM (sensu Clowes, 1994,
2000; Heimsch and Seago, 2008), and the pattern of cortical
development from a tiered RAM further illustrates a monocotlike root.
In overcoming some of the questions which Les and
Schneider (1995) posed about the lack of solid evidence for
nymphaealean and monocot phylogenetic connections, we
argue that there is no stronger anatomical evidence for a
Nymphaealean – monocot connection than the RAM and
The endodermis is a well-defined structural feature of angiosperm roots (Kroemer, 1903; Van Fleet, 1950; Wilson and
Peterson, 1983; Seago and Marsh, 1989; Seago et al., 1999b;
Soukup et al., 2005; Meyer et al., 2009), except possibly in
holoparasites (Kuijt and Bruns, 1987). A hypodermis is the
outermost cell layers of the cortex derived by periclinal divisions in the outer ground meristem (Seago and Marsh,
1989). When CBs are present and SL are also always
present, the cell layer(s) is termed exodermis (Kroemer,
1903; Wilson and Peterson, 1983; Perumalla et al., 1990;
Peterson and Perumalla, 1990; Seago et al., 1999b).
Multiseriate exodermis is much more common in monocots
than in eudicots (Seago et al., 1999a, b; Peterson and
Perumalla, 1990). Two different cell types can occur in exodermis – long cells and short cells; Shishkoff (1987) reported
no dimorphic hypodermis in Nymphaeales (see also Seago
et al., 2000b) and Laurales, but found them in Magnoliales
and in basal eudicot Ranunculales (not in the Papaveraceae,
however). Dimorphic hypodermis as seen in Allium cepa
(Fig. 5K) is fairly common in monocots. The exodermis and
its passage cells can have major effects on root– fungus associations (e.g. Baylis, 1972; Brundrett, 2002).
There have been analyses of root structures with regard to
their application to systematics (e.g. French, 1987a, b;
234
Seago & Fernando — Anatomical aspects of angiosperm root evolution
Keating, 2002), but differences in interpretations present some
problems. Kauff et al. (2000) found a dimorphic rhizodermis
in Hydrocharitaceae and Pontederiaceae, but Seago et al.
(1999a, 2000a) showed developmentally that only the outer
layer is the epidermis. Hydrocharis (Fig. 5I) does not have
an exodermis, and Pontederia has a uniseriate exodermis as
the outer layer of a dimorphic or trimorphic hypodermis
whose inner layers are only suberized (see related Eichhornia,
Fig. 5E).
Vascular tissues
The similarities between members of the Nymphaeales and
the Acorales have been noted with regard to xylem cell structure
(Schneider and Carlquist, 1995, 2002; Carlquist and Schneider,
1997) as well as cortex structure (Seago et al., 2005). Monocots
have far more aquatic/wetland species and families (Les and
Schneider, 1995; Van der Valk, 2012) than do eudicots, and
their roots, mostly adventitious, are often polyarch. In the
basal angiosperms, two of the families, Cabombaceae and
Hydatellaceae, have predominantly monarch roots, while the
Nymphaeaceae are dominated by species with mainly polyarch
roots, as are Acorus (Acoraceae), sister to the rest of the monocots, and the Araceae (Keating, 2002). Most of the remainder of
the monocots are polyarch, except for aquatic families such as
Hydrocharitaceae (Seago et al., 1999a) and Lemnaceae
(Landolt, 1998), plants with tiny roots which have triarch or
monarch steles, respectively.
According to Metcalfe and Chalk (1950a, b), Popham
(1966), Esau (1977) and Metcalf (1987), eudicots are generally
depicted as having two to six poles or strands of primary
xylem and phloem (often, apparently, diarch in young lateral
roots; Byrne and Heimsch, 1968; Byrne, 1973). It seems that
diarchy is more common in primary roots (derived from radicles), at least in the basal angiosperms. That some wetland
eudicots at the base of the core eudicots (Gunnera) and near
the base of the basal eudicots (Nelumbo) are strikingly polyarch, such as Nymphaeaceae and the vast majority of monocots, raises interesting questions. Possibly, plants evolving in
aquatic/wetland conditions retain and express the genes necessary for adventitious root production and polyarchy more
frequently than non-aquatic plants. The greater the number
of poles or strands of xylem and phloem (heptarchy and
above), the less likely it is that secondary growth may occur,
whereas diarch to hexarch patterns can lead more easily to secondary growth.
Primary and adventitious roots
Since so many species, especially among basal angiosperms
(including Nymphaeales, e.g. Friedman et al., 2012) and eudicots, have two cotyledons with a diarch vascular pattern in
primary and other roots, except in the nymphaealean
Trithuria, leading to the possibility that diarchy is strongly
related to the dicotyledonary condition, then one might
expect that monocot primary roots might have a monarch
primary or seminal root. Such is clearly not the case; and,
too many basal angiosperms and magnoliids have patterns
other than diarchy.
Another aspect of development and structure which should
be examined more closely is the state of embryo development
and structure at the time of maturation and germination.
Amborellales, Nymphaeales and Austrobaileyales have very
small embryos with little differentiation (Martin, 1946; Tobe
et al., 2000; Friedman et al., 2012; see also Taylor et al.,
2006, for fossil Nymphaeaceae). This might be important to
the balance between a primary root system and adventitious
root systems, to the relative state of development in primary
roots vs. adventitious roots and to differences in origin of
monocots and eudicots from basal angiosperm ancestors.
Most eudicots, when producing adventitious roots, form
them from more or less typical eudicot vascular patterns in
stems, bundles in one ring with a remnant procambial strand
or incipient vascular cambium. Most monocots, on the other
hand, form adventitious roots from stems with scattered vascular bundles or two or more rings of vascular bundles, so that
one could argue that it is the number of available vascular
bundles that produces the greater number of xylem and
phloem poles in monocot roots. Thus, vascular patterns in
embryonically produced roots might reflect vascular bundle
distributions of their stems. The contributions of molecular
genetics will have a major impact on our understanding of evolution of vascular patterns in roots (see Scarpella and Meijer,
2004).
Root symbioses, mycorrhizae and nodules
On the matter of mycorrhizae, after Baylis (1972), Simon
et al. (1993) and Cairney (2000), Brundrett’s (2002) thesis
of rhizomes evolving into roots related fungal inhabitations
to root evolution. Brundrett offered possible root structural
features needed to accompany the evolutionary pathways.
Mycorrhizal roots can sometimes be extremely modified
(e.g. Imhof, 1997, 2001). For nodules, the study of Soltis
et al. (1995) confirmed that there are only two eudicot families
(Fabaceae, Ulmaceae) with Rhizobium nodules and eight families (Betulaceae, Casuarinaceae, Elaeagnaceae, Myricaceae,
Rhamnaceae, Rosaceae, Datiscaceae and Coriariaceae) with
Frankia actinomycetes. A recent study by Markmann et al.
(2008) suggests how the evolutionary path may have involved
the same genes in both nodulating bacteria, but the root structural paths have not been well addressed. Heimsch and Seago
(2008) and Seago et al. (2005) briefly discussed the ramifications of RAM and cortex structure, respectively, in relation to
nodule formation. It should be noted that these families with
nodulating roots are not closely associated with basal angiosperms or basal eudicots, and none is found in the monocots
where epidermal origin is associated with cortex, not lateral
rootcap; roots with bacterial symbioses seem likely to represent a derived condition in angiosperms.
In summary, root anatomy offers many interesting perspectives on developmental patterns, systematics and evolutionary
relationships but, since their structure can vary depending on
the type of experimental conditions, their importance is
often less appreciated. However, when roots are examined
based on their typical habitats, they can be useful when comparing groups of plants. Therefore, based on the information
presented in this overview, there appears to be a general
trend in angiosperm root structure (see summarized
Taxa
Habitat
Types of roots
examined
Types of
stele
Stage of
growth
Endodermis
Mid-cortex
pattern
Aerenchyma
Hypodermis exodermis
RAM
Amborellales
Terrestrial
Adventitious;
lateral
Diarch;
triarch
Primary;
secondary
All with CBs and SL
Non-radial
None
All with CBs and SL
Epidermis-lateral rootcap;
common initials, irregular
epidermis
Epidermis-cortex
Nymphaeales
Aquatic
Adventitious
Adventitious;
lateral
Some CBs; some CBs
and SL
All with CBs SL;
some dilatated
Radial;
non-radial
Non-radial
All with CBs and SL
Terrestrial
Primary
only
Primary;
secondary
Expansigenous
Austrobaileyales
Monarch
polyarch
Diarch
tetrarch
None
All with CBs and SL
Magnoliids
Terrestrial
Diarch to
hexarch
Primary;
secondary
All with CBs and SL;
some dilatated
Non-radial
None
All with CBs and SL;
some dilatated
Monocots
Aquatic
Terrestrial
Primary;
adventitious;
lateral
Adventitious
Primary; lateral
Polyarch
Triarch in a
few
Primary
only
Radial;
non-radial
Expansigenous;
schizogenous;
lysigenous
None; some CBs and
SL; many CBs, SL and
secondary walls
Epidermis-cortex
Eudicots
Terrestrial
Primary; lateral
Schizogenous;
lysigenous;
expansigenous
None; some CBs and
SL; some CBs, SL and
econdary walls; some
dilatated
Epidermis-lateral rootcap
Adventitious
Primary;
mostly
secondary
Radian;
non-radial
Aquatic
Diarch to
hexarch
Polyarch in
some basal
aquatics
Some only CBs; some
CBs and SL; many
CBs, SL and
secondary walls
Many CBs; some CBs
and SL; some CBs,
SL and secondary
walls
Epidermis-cortex;
common initials, irregular
epidermis
Common initials, irregular
epidermis
Seago & Fernando — Anatomical aspects of angiosperm root evolution
TA B L E 1. Summary of selected, but typical anatomical features of angiosperm roots (including RAMs from Heimsch and Seago, 2008)
235
236
Seago & Fernando — Anatomical aspects of angiosperm root evolution
information in Table 1) and, in general, we note that the
Amborellales and magnoliids have many root structural features like those of eudicots, whereas the Nymphaeales roots
are strikingly similar to those of the monocots, especially
basal monocots such as Acorales. The Austrobaileyales are enigmatic and have root structural features which do not align
easily to either monocots or eudicots. Clearly, the basal
angiosperms require far more anatomical examination to corroborate the findings of molecular phylogenetic analyses.
AC KN OW LED GEMEN T S
For their assistance in various ways, we thank Arnold Salazar,
Aleš Soukup, Daryl Enstone, Christopher Meyer, Chaodong
Yang, Carol Peterson, Marilyn Seago, Edita Tylová,
Alexander Lux, Daniel Gladish, Olga Votrubová and two anonymous reviewers. J.L.S. received a travel grant from
SUNY Oswego Office of International Education to support
the ISRR trip. The late Charles Heimsch is specially noted
because he instilled in J.L.S. the idea that root evolution in
angiosperms is very important.
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Ayensu ES. 1972. Anatomy of the monocotyledons. VI. Dioscoreales. Oxford:
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Barlow PW. 1994. Structure and function at the root apex – phylogenetic and
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