Annals of Botany Page 1 of 14
doi:10.1093/aob/mcw006, available online at www.aob.oxfordjournals.org
Root evolution at the base of the lycophyte clade: insights from
an Early Devonian lycophyte
Kelly K. S. Matsunaga* and Alexandru M. F. Tomescu
Department of Biological Sciences, Humboldt State University, Arcata, CA, USA
* For correspondence. E-mail kkm31@humboldt.edu
Received: 17 July 2015 Returned for revision: 21 October 2015 Accepted: 30 November 2015
Key words: Devonian, root evolution, rooting system, lycophyte, fossil, Wyoming.
INTRODUCTION
Rooting systems are a fundamental component of modern plant
body plans, responsible for anchorage and uptake of water and
nutrients from the substrate. The evolution of rooting systems
transformed terrestrial ecosystems by influencing soil weathering processes and nutrient cycling at a global scale (Algeo and
Scheckler, 1998; Berner and Kothavala, 2001; Bergman et al.,
2004; Taylor et al., 2009). Rooting systems of modern plants
exhibit a wide range of morphological diversity, and consist of
roots, modified shoots or both. Roots are recognized as axial organs with radial symmetry, endogenous origin, root hairs and a
root cap (Raven and Edwards, 2001; Kenrick and StrulluDerrien, 2014). Throughout this article the term root is used in
this strict sense and is not applied to other organs that have a
rooting function. In many plants the rooting system consists
only of roots, but in numerous seed-free plants and angiosperms
modified stems called rhizomes also play a key role in anchoring the plant, and often also produce roots. Other plants lack
roots entirely. For instance, the lycophyte Isoetes has a rooting
system consisting of a highly modified shoot whose appendages
(‘rootlets’) are homologous to leaves (Rothwell and Erwin,
1985; Raven and Edwards, 2001; Rothwell et al., 2014),
whereas the rooting system of Psilotum consists of rhizoidbearing undifferentiated axes (Gifford and Foster, 1989).
While organs that can be recognized as roots are ubiquitous
among vascular plant lineages, not all of these organs are homologous. Roots evolved independently at least twice in the
two major clades of vascular plants – the lycophytes and
euphyllophytes (sensu Kenrick and Crane, 1997; Raven and
Edwards, 2001; Boyce, 2005; Seago and Fernando, 2013;
Kenrick and Strullu-Derrien, 2014). In these groups, an independent origin of roots is inferred from the fossil record and developmental differences. Lycophyte and euphyllophyte stem
groups lacked roots (although they were not entirely devoid of
other types of rooting structures; Kenrick, 2002; Kenrick and
Strullu-Derrien, 2014), and so the most parsimonious hypothesis is that the common ancestor of the two clades was also rootless (Friedman et al., 2004; Boyce, 2005). Developmental
differences also support independent origins: euphyllophyte
roots branch endogenously from cells of the pericycle or endodermis, whereas lycophyte roots branch apically through division of the meristem (Gifford and Foster, 1989; Friedman et al.,
2004). However, despite the evidence indicating that they are
not homologous, lycophyte and euphyllophyte roots share
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Background and Aims The evolution of complex rooting systems during the Devonian had significant impacts
on global terrestrial ecosystems and the evolution of plant body plans. However, detailed understanding of the pathways of root evolution and the architecture of early rooting systems is currently lacking. We describe the architecture and resolve the structural homology of the rooting system of an Early Devonian basal lycophyte. Insights
gained from these fossils are used to address lycophyte root evolution and homology.
Methods Plant fossils are preserved as carbonaceous compressions at Cottonwood Canyon (Wyoming), in the
Lochkovian–Pragian (411 Ma; Early Devonian) Beartooth Butte Formation. We analysed 177 rock specimens
and documented morphology, cuticular anatomy and structural relationships, as well as stratigraphic position and
taphonomic conditions.
Key Results The rooting system of the Cottonwood Canyon lycophyte is composed of modified stems that bear
fine, dichotomously branching lateral roots. These modified stems, referred to as root-bearing axes, are produced at
branching points of the above-ground shoot system. Root-bearing axes preserved in growth position exhibit evidence of positive gravitropism, whereas the lateral roots extend horizontally. Consistent recurrence of these features
in successive populations of the plant preserved in situ demonstrates that they represent constitutive structural traits
and not opportunistic responses of a flexible developmental programme.
Conclusions This is the oldest direct evidence for a rooting system preserved in growth position. These rooting
systems, which can be traced to a parent plant, include some of the earliest roots known to date and demonstrate
that substantial plant–substrate interactions were under way by Early Devonian time. The morphological relationships between stems, root-bearing axes and roots corroborate evidence that positive gravitropism and root identity
were evolutionarily uncoupled in lycophytes, and challenge the hypothesis that roots evolved from branches of the
above-ground axial system, suggesting instead that lycophyte roots arose as a novel organ.
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Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
MATERIAL AND METHODS
The lycophyte fossils that form the basis of this study were recovered from the Beartooth Butte Formation at Cottonwood
Canyon, Wyoming (Big Horn Co., 44 510 5100 N, 108 020 4600 W).
There, plant fossils occur in dense autochthonous and parautochthonous assemblages and in situ preservation is frequent.
The lycophyte is preserved as coalified to oxidized compressions and impressions.
Throughout northern Wyoming and southern Montana, the
Beartooth Butte Formation displays geometries reminiscent of
channel-fill deposits, characterized by long narrow bodies of
sediment that are lenticular in cross-section. The deposits consist primarily of dolomitized siltstone and shale with dolomitized sandstone interbeds (Sandberg, 1961, 1967; Caruso and
Tomescu, 2012). The unit contains fish, eurypterid and terrestrial plant fossils, as well as encrusting microconchid lophophorates (Dorf, 1933, 1934; Schultes and Dorf, 1938; Denison,
1956; Elliot and Johnson, 1997; Tetlie, 2007; Lamsdell and
Legg, 2010; Lamsdell and Selden, 2013; Caruso and Tomescu,
2012). Based on its geometry and fossil content, the unit has
been interpreted as fresh- and brackish-water deposits of estuarine to fluvial environments (Dorf, 1934; Denison, 1956;
Sandberg, 1961), an interpretation corroborated by limited isotope data (Fiorillo, 2000). Palynological analyses by D. C.
McGregor (reported by Tanner, 1983) suggest a late
Lochkovian – early Pragian age for the plant fossil layers at
Cottonwood Canyon, independently confirmed by fish biostratigraphy (Elliot and Johnson, 1997).
This study used 177 rock specimens held in collections curated at the US National Museum of Natural History –
Smithsonian Institution (USNM), the Denver Museum of
Nature and Science (DMNH), the Field Museum of Natural
History (FMNH), the University of Kansas Biodiversity
Institute (KU) and Humboldt State University (HPH). The
specimens originate from a 15- to 18 -m-thick section and,
within it, from locations along the outcrop no more than 10 m
apart. Although not all specimens were collected by us, we
know they all originate from the same stratigraphic level because accessibility issues in the field, at Cottonwood Canyon,
preclude collection of specimens from other levels and
locations.
High-resolution images obtained in parallel with direct examination of collection specimens were compiled in a database
and used for morphological and morphometric analyses. When
needed for resolution of morphological detail, selected specimens were obtained on loan from KU and NMNH.
Specimens of the Cottonwood Canyon lycophyte were assigned by Tanner (1983) to Drepanophycus devonicus.
However, examination of museum specimens and of our own
recently excavated material indicates that while the plant is indeed a drepanophycalean lycophyte, assignment to D. devonicus should be re-evaluated. Whole-plant reconstruction and
taxonomic revision of this lycophyte involve much additional
information and discussion of Cottonwood Canyon fossils, and
are therefore not addressed here.
Fragments of cuticle were removed using cellulose acetate
peels taken from the surface of rock specimens. Peels were
placed in 05 % hydrochloric acid to dissolve residual minerals
before mounting on slides using Eukitt (O. Kindler, Freiburg,
Germany). No clearing of cuticles was necessary.
The material was imaged using a Nikon Coolpix E8800 digital camera mounted on a Nikon Eclipse E400 microscope, an
Olympus DP73 digital camera mounted on an Olympus SZX16
dissecting microscope, an LG G4 cell phone camera and an
Epson Perfection 4490 Photo scanner. Measurements were obtained using ImageJ (National Institutes of Health, Bethesda,
MD, USA). Images were processed using Pixelmator 3.4
(Pixelmator Team, London, UK).
RESULTS
Body plan
The body plan of the Cottonwood Canyon lycophyte consists of
three distinct types of axial organ found in physical connection:
robust leafy stems, smaller leafless axes and fine, dichotomously branching lateral appendages borne exclusively on the
leafless axes. We interpret these lateral appendages as roots, as
discussed below, and for clarity we hereafter refer to them as
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defining characters, listed above, that distinguish them from
other organs.
Although the independent origin of roots in lycophytes and
euphyllophytes is widely accepted, fundamental questions on
how roots evolved within these lineages remain unanswered.
For instance, what is the homology of these organs – were they
derived from the undifferentiated axes of the tracheophyte stem
groups, or did they arise as novel organs? Lycophyte roots appear earlier in the fossil record than those of euphyllophytes
(Boyce, 2005; Raven and Edwards, 2001) and several authors
have suggested that they evolved from aerial stems or axes
(Stewart and Rothwell, 1993; Gensel and Berry, 2001; Gensel
et al., 2001; Seago and Fernando, 2013). This hypothesis stems
from the prevalence among extinct lycophytes of rooting systems derived from branches of the above-ground axial system.
Such occurrences are documented in basal lycophyte stem
groups (zosterophylls, Asteroxylon) and isoetalean lycophytes
(Kidston and Lang, 1920; Rothwell and Erwin, 1985; Gensel
et al., 2001; Hao et al., 2010). Attempts to address such questions on root evolution are frustrated by the rarity of wellpreserved rooting systems in the fossil record, especially in
early vascular plants. Moreover, although some extensive early
rooting systems have been documented (Elick et al., 1998;
Poschmann and Gossmann, 2014) their parent plants are not
known.
Here we document the rooting system of a basal lycophyte
from the Early Devonian (late Lochkovian – early Pragian;
approx. 411 Ma) Beartooth Butte Formation exposure at
Cottonwood Canyon, in Wyoming. Both the above-ground
shoot system and the rooting system of this plant (hereafter,
Cottonwood Canyon lycophyte) are preserved in situ, providing
rare insights into the growth habit and overall architecture of
the rooting system, as well as the structural homology of these
rooting organs. This is the oldest occurrence of a rooting system
preserved in growth position, in connection with a parent plant.
We discuss it in the context of the current understanding of the
fossil record and morphology of roots, to address questions on
lycophyte root evolution and homology.
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
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such. The leafless axes subtending the roots are referred to as
root-bearing axes.
The leafy stems are up to 34 mm wide (mean 15 mm;
n ¼ 567) and bear loose helices of small triangular leaves
(1–7 mm) (Fig. 1). A narrow central vascular strand (stele)
(1–2 mm) is conspicuous in most specimens (Fig. 1). The leafless root-bearing axes are much narrower on average than stems
(2–8 mm wide; mean 44 mm; n ¼ 452) and possess a thin central stele (05–15 mm) (Fig. 2). These axes are produced by
branching of the leafy stems, described in detail below.
Segments of root-bearing axes range from 3 mm to 13 cm in
length, and the combined length of all the segments used in this
study is approx. 14 m.
Lateral roots, occurring exclusively on root-bearing axes,
have a narrow central vascular strand that is continuous with
that of the subtending axis (Figs 2 and 5A). Root arrangement
along axes ranges from alternate to opposite (Fig. 2), with root
tufts spaced from 2 to 40 mm apart (average distance 11 mm;
n ¼ 161). Segments that lack roots can be recognized as rootbearing axes by their size, the absence of leaves, the conspicuous narrow central stele and, where preserved, characteristic
epidermal anatomy (described below). When root preservation
is incomplete, the position of roots along the axis is revealed by
protruding root bases (Fig. 2E, F) or by the presence of root
vascular traces in the cortex. Root vascular traces exhibit a
characteristic pattern, with divergence angles <90 (Fig. 2E,
F). While root-bearing axes are leafless overall, their bases can
bear sparse reduced leaves near their divergence from leafy
stems (Figs 3A and 7B). Because of this, root-bearing axes that
do not show attachment to leafy stems, but have sparse minute
leaves, probably represent basal regions (Fig. 7H).
Root morphology was documented based on 615 root tufts
observed on 310 root-bearing axes. The roots are fine (04–
07 mm thick) and branch dichotomously (Fig. 4). Darker regions observed occasionally at their tips may represent root
caps (Fig. 4A–C). No root hairs were observed on the roots.
This could be due to the delicate nature and low preservation
potential of root hairs, or to the rarity of preserved root tips in
the fossil material (root hairs are only found immediately behind the root apex). Alternatively, the Cottonwood Canyon
lycophyte may not have produced root hairs.
The branching architecture of the roots is widely variable.
Dense branching close to the root base results in a tufted habit
wherein numerous roots seem to arise from a thick base up to
3 mm wide (Fig. 4F, see also Fig. 3B). In other instances, more
widely and regularly spaced dichotomies produce roots with
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FIG. 1. Leafy stems of the Cottonwood Canyon lycophyte. (A) Leafy stem and smaller root-bearing axis. Note narrow central stele of leafy stem (arrow) and bases of
root tufts on root-bearing axis (arrowheads). Scale bar ¼ 20 mm. HPH 229. (B) Stem mat consisting of numerous leafy stems in shale layer. Although the vertical dimension is not shown, this layer hosts many interwoven stems separated by millimetre to submillimetre shale laminae over a thickness of several centimetres. Scale
bar ¼ 40 mm. KU D1806. (C) Leafy stem. Note central stele (arrow) and leaves with visible veins (arrowheads). Scale bar ¼ 20 mm. FMNH PP15972.
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Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
thinner bases (<2 mm) (Figs 2B and 4D, G). These two situations are end-points of a continuous series, as seen, for example,
in roots that show dense branching proximally and greater distance between branches distally (Fig. 4E). The largest root tufts
observed extend as far as 20 mm laterally from the subtending
axes and have up to five orders of branching. Seemingly isolated root tufts that are found without clear attachment to rootbearing axes can be recognized as belonging to the Cottonwood
Canyon lycophyte by their size, thin stele and characteristic
branching architecture (Fig. 5).
Leafy stems and root-bearing axes are distinguished by their
epidermal anatomy. In leafy stems, epidermal cells are isodiametric to slightly elongate longitudinally, 37–66 46–96 mm,
and stomata are abundant (Fig. 6A–D). In contrast, epidermal
cells of root-bearing axes are narrow and elongate-rectangular,
22–31 95–155 mm (Fig. 6F, H). When present on root-bearing
axes, stomata are similar to those of the leafy stems but are
sparse and irregularly distributed (Fig. 6E). No cuticle could be
recovered from roots and their epidermal anatomy is unknown
(Fig. 6G).
Stomata on leafy stems are surrounded by six or seven epidermal cells. The size and shape of these cells are variable,
ranging from cells that have the appearance of subsidiary cells
to cells that look the same as ordinary epidermal cells (Fig. 6B–
D). The rare stomata found on root-bearing axes are surrounded
by elongate cells characteristic of the epidermis of these axes
(Fig. 6E). Owing to the variability of stem stomata, and to the
clear lack of subsidiary cells on root-bearing axes, stomata of
the Cottonwood Canyon lycophyte are interpreted as
anomocytic.
Branching
Branching of the plant consists exclusively of K-branches.
These are produced only on leafy stems; branching has never
been observed in the root-bearing axes, despite the large sample
analysed. K-branching characterizes several early lycophytes
(e.g. Drepanophycus, Zosterophyllum) and consists of two
closely spaced dichotomies, the second of which produces two
branches (hereafter referred to as ‘arms’) that diverge at wide
angles, resulting in a K-shaped morphology (Fig. 7A, B). In the
Cottonwood Canyon lycophyte, each K-branch generates a
leafy stem and a root-bearing axis (Figs 3 and 7B). All
K-branches are vascularized by a thick vascular strand, which
diverges from the stele of the main stem at approximately 90
and bifurcates to supply the two arms of the K-branch (Figs 3B
and 7).
K-branches were observed in several stages of development.
Some occur as lateral buds, which are K-branch primordia. The
buds are squat and covered in small leaves (Fig. 7E–G). A central furrow and apical bifurcation of the vascular strand observed in some of the buds indicates the presence of two apical
meristems corresponding to early stages of the second dichotomy (Fig. 7E–G). Later developmental stages are represented
by K-branches in which only one arm is developed and bears a
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FIG. 2. Root arrangement and variable preservation of root-bearing axes and attached roots in the Cottonwood Canyon lycophyte. Root tufts range from intact (A, B)
to completely absent due to poor preservation or to the fact that they are covered by the rock matrix (F). The tips of some otherwise well-preserved roots are not seen
because they depart into the rock matrix (C, D). In other specimens only the bases of root tufts are preserved (E), or roots are not preserved at all and their position is
indicated only by root traces in the cortex of subtending axes (F; arrow); note similar root vascular traces in the cortex of other root-bearing axes (C, D; arrows).
Preservation of the root-bearing axes ranges from coalified (B, D) to fully oxidized (A). (C), (E) and (F) show partial oxidation of the stele. Note alternate and opposite root arrangement on the same axis in (C) and (E). Scale bars ¼ 5 mm. Specimens: KU D1813 (A), KU D1618b (B), KU D1804 (C), KU D876b (D), KU D1281b
(E), KU D1166a (F).
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
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FIG. 3. Root-bearing axes produced by K-branching in the Cottonwood Canyon lycophyte. (A) Part (top) and counterpart (bottom) of specimen showing a leafy stem
with a root-bearing axis diverging from it. Note impression of the stele of the root-bearing axis in the counterpart (white arrow) demonstrating continuity between
the vasculature of the main stem and root-bearing axis. The root-bearing axis has several reduced leaves at the base (black arrowheads) and four root tufts (black arrows). It is unclear if the other arm of the K-branch is present, but the curvature of the stele in the main stem (white arrowhead) suggests the arm, if developed, may
overlap the main stem. Scale bar ¼ 10 mm. HPH 356. (B) Leafy stem with two K-branches (white arrows). The steles of the main stem, K-branches and root traces
are oxidized, revealing the details of branching. One K-branch (at left) produces one arm, which is cut off at the edge of the rock specimen, and a leafy bud (black arrowhead). The other K-branch (at right) produces one arm that is cut off at the edge of the rock specimen and a root-bearing axis, which is folded over itself (at asterisk). Five root tufts (black arrows) are present along this root-bearing axis; note that root traces diverge away from the base of the axis, in the direction of its apex
(top). Images of the partially preserved portions of the part (D1812a) and counterpart (D1812b) of this specimen have been merged digitally (boxed area, at right) to
show continuity between the root-bearing axis and the main stem. Scale bar ¼ 10 mm. KU D1812.
dormant bud at its base (Fig. 7C, D), and complete K-branches
exhibiting full development of both arms (Fig. 7A, B).
In situ preservation and downward growth of root-bearing axes
The Cottonwood Canyon lycophyte is frequently preserved
in situ, forming thick layers of plant material. In situ
preservation is supported by several observations. First, the
lycophyte forms extensive, dense mats of interwoven stems in
finely laminated shales devoid of other plant taxa (Fig. 1B).
Second, organic detritus indicative of transport is absent from
these stem mat layers. Third, the lycophyte shoot systems and
attached root-bearing axes are very well preserved. Finally,
the stem mat layers recur stratigraphically, alternating with
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Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
hard-cemented siltstones (Fig. 9A) that contain transported
fragments of plant material, fish plates and other organic detritus (Fig. 8A). The stratigraphic recurrence of these stem mat
layers, which lack other organic detritus, supports their interpretation as in situ, as it is unlikely that well-sorted plant material
was consistently deposited in the same location repeatedly
through time.
Vertical breaks in the siltstones that alternate with the stem
mats reveal in situ root-bearing axes (Fig. 8). These axes are
orientated vertically and extend downward from the stem mats
at least 12 cm (Fig. 9B, C), crossing bedding planes (Fig. 8B,
D). Like the horizontal root-bearing axes, these vertical axes
have a thin central stele and lateral, dichotomously branching
roots, which are typically compressed on horizontal bedding
planes (Figs 8A, C and 4F, G). The arrangement and divergence
of lateral roots from the vertical axes are identical to those of
the horizontal root-bearing axes preserved on bedding planes.
The direction of growth of the vertical root-bearing axes is
revealed by two types of observations on specimens from rock
samples with known vertical orientation. First, in horizontal
root-bearing axes, decurrent root traces diverge from the axis
stele laterally and in the direction of the apex (Fig. 3B). In vertical root-bearing axes, root traces diverge laterally and downwards from the axis stele (Fig. 8F), and therefore these axes
were growing downwards. Second, even in cases where the
root traces are not visible through the cortex, the roots themselves diverge downwards at wide angles from the subtending
axes before becoming horizontal (Fig. 8B), consistent with
downward growth of the root-bearing axes. Together, these indicate that the growth trajectory of root-bearing axes was
downward.
DISCUSSION
Conspecificity of organs
The conspecificity of specimens used in this study is supported
by several lines of evidence. First, the frequent co-occurrence
of in situ root-bearing axes and leafy stems in layers devoid of
any other taxa provides strong circumstantial evidence for conspecificity. Second, where leafy stems and root-bearing axes
co-occur, they exhibit identical preservation, such as comparable degrees of differential preservation of cortex and stele, or
comparable degrees of oxidation. These similarities in preservation suggest that both types of organs have similar anatomy and
chemistry, and thus support conspecificity. Third, despite being
different in size, leafy stems and root-bearing axes do overlap
morphologically. Both organs possess a narrow central stele
that often has longitudinal striations potentially related to its
anatomy. Moreover, some segments of root-bearing axis bear
sparse minute leaves similar to those found on bases of
K-branches (Figs 3A, 7B, H); these segments probably represent proximal fragments of root-bearing axes. Fourth, unequivocal evidence of conspecificity comes from specimens showing
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FIG. 4. Roots of the Cottonwood Canyon lycophyte. (A–C) Roots with darkened apices that may represent root caps (arrows). Part (B) and counterpart (C) of specimen are shown to demonstrate that all three roots have darkened apices. (D–G) Roots showing various degrees and patterns of branching. Note the thin central stele
clearly visible in (D), and the dense branching at the base of roots in (F), which have a tufted appearance. (F) and (G) illustrate root tufts diverging in opposite directions, in a horizontal plane, from vertical root-bearing axes (asterisks) exposed in cross-section on the bedding plane. Scale bars ¼ 5 mm. Specimens: HPH 27 (A),
KU D872a (B), KU D872b (C), KU D1616b (D), KU D1625h (E), KU D1153 (FG), KU D1814 (G).
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
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physical attachment of leafy stems and root-bearing axes
(Fig. 3).
gravitropic subterranean growth – the rhizomorphic clade
(Rothwell and Erwin, 1985).
Homology of the root-bearing axes
Root recognition in the fossil record – a conundrum
Although the root-bearing axes grow downwards, several of
their features indicate that they are modified stems and not
roots. First, they are parts of K-branches, which arise from lateral buds that are consistently bisected into two identical leafy
apices. This morphology indicates that the buds branch apically
to produce the two K-branch arms. Thus, the root-bearing axes
produced by K-branching arise exogenously, as products of
shoot apical branching, and not endogenously like roots.
Second, despite being predominantly leafless, root-bearing axes
produce leaves early in their development. The axes originate
as leafy buds (Fig. 7C–H) and, as a result, bear sparse reduced
leaves at their base (Figs 3A and 7B) – no roots have ever been
known to produce leaves. Finally, the presence of cuticle and
stomata on the epidermis of root-bearing axes (Fig. 6E–H) is
consistent with stem homology. Moreover, the thick cuticle
comparable to that of the stems suggests that root-bearing axes
were not involved in water absorption. Together, all these features are consistent with stem homology of the root-bearing
axes, despite their positively gravitropic subterranean growth.
This is not surprising, considering that the lycophyte clade includes one other instance of shoot homologues with positively
The roots of extant plants are traditionally defined and recognized based on a set of morpho-anatomical criteria: radial symmetry, endogenous origin, positive gravitropism, root hairs and
a root cap (Gensel et al., 2001; Raven and Edwards, 2001;
Kenrick and Strullu-Derrien, 2014). However, because recognizing these characters requires detailed anatomical and developmental data, some of these criteria are difficult, if not
impossible, to apply to fossils (Lyon and Edwards, 1991;
Edwards, 1994; Gensel et al., 2001). Further complicating the
situation, some early vascular plants have rooting structures, derived from stems or axes, that are not roots (e.g.
Zosterophyllum; Hao et al., 2010). As a result, most Early
Devonian root-like structures have been treated cautiously, as
none of them meets all of the root recognition criteria (e.g.
Gensel et al., 2001).
Studies of the root fossil record are thus presented with a
problem: on the one hand, criteria are necessary to ensure fossils provide accurate data for studying character evolution; on
the other hand, the traditional root recognition criteria are not
applicable to most fossils due to their mode of preservation.
Consequently, for the purposes of identifying fossil roots, the
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FIG. 5. Comparison of roots attached to root-bearing axes of the Cottonwood Canyon lycophyte (A, C) with those detached from or not visibly attached to axes
(B, D). The close similarity in morphology and branching architecture indicates that the isolated root tufts belong to the Cottonwood Canyon lycophyte.
Scale bars ¼ 5 mm. Specimens: KU D1804 (A), KU D1631a (B), KU D1618b (C), KU D1631b (D).
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Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
traditional morpho-anatomical criteria for root recognition are
usually impractical. To circumvent this problem, we propose a
different approach that we apply to assess the homology of the
roots of the Cottonwood Canyon lycophyte, which in the following discussion will be referred to as ‘lateral appendages’.
This approach considers two aspects: (1) alternative potential
homologies of the lateral appendages, i.e. could these appendages be stems, leaves or a novel organ type; and (2) additional
characters that the lateral appendages share with roots.
Did the Cottonwood Canyon lycophyte have roots?
Stem homology of the lateral appendages of root-bearing
axes is rejected because they do not bear leaves and are different from both types of stems produced by this plant (leafy stems
and root-bearing axes) in size and mode of branching. Several
characters of the lateral appendages are also inconsistent with
leaf homology: irregular arrangement along the root-bearing
axes, indeterminate growth and irregular branching. While appendages homologous to leaves and displaying indeterminate
growth and irregular branching are known in the lycophyte
clade (rhizomorphic lycopsids; Karrfalt, 1980; Rothwell and
Erwin, 1985), those appendages have regular arrangement and
undergo abscission, unlike the lateral appendages of the
Cottonwood Canyon lycophyte.
If the lateral appendages are not stems or leaves, the only
other alternatives are that they represent roots or a novel type of
organ. The lateral appendages do share several features with
roots. First, they are exclusively subterranean organs whose
morphology is consistent with absorptive functions. Second, the
lateral appendages lack a cuticle. Film pulls of root-bearing
axes and their lateral appendages show that the cuticle, well
preserved along the axis, ends abruptly at the base of the lateral
appendage (Fig. 6G). This indicates the appendages had very
thin cuticle, if any, which is a common feature of roots that are
actively involved in water uptake (Esau, 1977). Third, some
specimens have darkened apices, which may represent preserved root caps (Fig. 4A–C). Finally, these lateral appendages
exhibit the same apical branching architecture that characterizes
the roots of modern lycophytes such as Lycopodium and
Selaginella (Eames, 1936).
Our approach demonstrates that although they do not fit traditional criteria for root recognition, the lateral appendages of
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FIG. 6. Epidermal anatomy of leafy stems (A–D) and root-bearing axes (E–H) of the Cottonwood Canyon lycophyte. (A) Leafy stem epidermis showing isodiametric
epidermal cells and numerous stomata. Scale bar ¼ 200 mm. HPH 333. (B–D) Details of stomata on leafy stems. Note that epidermal cells surrounding guard cells
range from smaller than (B) to similar in size as regular epidermal cells (C, D). Also note variation in the size of epidermal cells surrounding the stoma in (C). Scale
bars ¼ 50 mm. HPH 76 (B, C), HPH 333 (D). (E) Detail of one of the rare stomata on a root-bearing axis. Note similarity in size and shape to the leafy stem stomata
in (B–D). Scale bar ¼ 50 mm. HPH 330. (F) Epidermis of root-bearing axis showing elongate epidermal cells. Note the absence of stomata. Scale bar ¼ 100 mm. HPH
330. (G, H) Film pull of cuticle of a root-bearing axis at the point of the attachment of a root. Note that whereas the cuticle of the root-bearing axis preserves cellular
patterns (H), the root consists of thick carbonaceous material. This sharp transition between the cellular pattern of the axis and the lack thereof in the root (arrow) is
interpreted as a lack of cuticle in the root. Scale bar ¼ 1 mm (G). Scale bar ¼ 200 mm (H). HPH 330.
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
Page 9 of 14
the Cottonwood Canyon lycophyte are most similar to roots.
However, despite sharing a set of developmental and functional
traits by which they can be recognized, roots are not homologous across tracheophytes. Consequently, any discussion of
morphological evolution that the appendages of the
Cottonwood Canyon lycophyte can inform should be framed
within the context of lycophyte root evolution. In this context,
the appendages of the Cottonwood Canyon lycophyte are most
similar to the roots of Lycopodium and Selaginella, which
renders their alternative interpretation as a novel organ less
parsimonious.
The rooting system – functional morphology
The Cottonwood Canyon lycophyte possesses a distinctively
complex rooting system that consists of two types of organs –
root-bearing axes and roots – that perform different functions
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Fig. 7. Different degrees of development of K-branches of the Cottonwood Canyon lycophyte. (A) Fully developed K-branch. Note the thick vascular trace diverging
from the stele of main stem at 90 angle. Scale bar ¼ 10 mm. KU D1039a. (B) Fully developed K-branch producing a leafy stem and root-bearing axis (arrow). Note
the smaller size and reduced leaves of the root-bearing axis; no roots are present on this segment of the axis. Scale bar ¼ 20 mm. FMNH PP15959. (C, D) K-branch
consisting of one fully developed arm and a leafy bud; in (D) parts of the specimen are traced for clarity. Note vascularization of the bud and fully developed arm.
Scale bar ¼ 10 mm. KU D932b. (E, F) Leafy bud; in (F) the vasculature is traced for clarity. Note the wide, squat shape of the bud and bifurcation of its vascular
strand, indicating presence of two adjacent apices. Scale bar ¼ 10 mm. KU D1471b. (G) Leafy bud exhibiting characteristic wide, squat shape and a slight central furrow (arrow) indicating presence of two adjacent apices. Scale bar ¼ 10 mm. DMNH 29591. (H) Root-bearing axis with reduced leaves (arrows). Basal segments of
root-bearing axes bear reduced leaves, as seen in (B) and Fig. 3A. Scale bar ¼ 10 mm. KU D1281a.
Page 10 of 14
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
(Fig. 10). The root-bearing axes have variable orientations, consistent with growth responses to external stimuli – in situ rootbearing axes are found growing downwards into the substrate
as well as horizontally, both on the ground surface and in the
substrate. The roots, by contrast, extend laterally from subtending axes up to only a couple of centimetres. They are delicate
and probably, alone, insufficient for anchoring the plant, especially given the large size of the above-ground stems.
Moreover, owing to their small size they were only capable of
exploring small volumes of substrate. In contrast, the rootbearing axes are extensive and robust enough to anchor the
plant and produce roots at various depths in the substrate, thus
allowing access to larger volumes of underground resources.
Together, these features indicate that in this plant the rootbearing axes, and not the roots, functioned as the primary organ
responsible for anchorage and substrate exploration. The roots
borne on these axes, while contributing minimally to anchorage, were the main absorptive organ.
The degree of functional complexity of this rooting system
provides direct evidence that by Pragian time, early vascular
plants had evolved mechanisms to actively explore their substrate utilizing complex foraging behaviours. In the outcrop at
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FIG. 8. Vertical in situ root-bearing axes of the Cottonwood Canyon lycophyte; all specimens shown in original stratigraphic orientation. (A) Oblique view of rock
specimen showing both vertical face (top) and lower horizontal face (bottom). In situ root-bearing axes preserved on the vertical face (top box) produce roots that diverge onto lower horizontal face (bottom box); upper box detailed in (B) and lower box in (C). Note abundant fragmented organic material on the lower horizontal
face of the rock specimen. Scale bar ¼ 10 mm. HPH 210. (B) Vertical face of rock specimen in (A) with two root-bearing axes that cross bedding planes. Note the
thin central stele in both axes (arrows) and numerous lateral roots (arrowheads) diverging from the axis at right. Diverging roots are compressed on horizontal planes,
but diverge with a downward curvature before becoming horizontal (e.g. at white arrowhead). One root tuft (not visible in this plane) diverges from the axis where it
intersects the lower horizontal face of the rock specimen (detailed in C). Scale bar ¼ 10 mm. (C) Horizontal face of rock specimen in (A) showing detail of root tuft
connected to the vertical root-bearing axis shown in (B). Note branching of the root, continuity with the vertical axis (asterisk) and thin central stele of root (arrow).
Scale bar ¼ 2 mm. (D) Vertical face of rock specimen with three root-bearing axes that cross bedding planes. All three axes are compressed in the vertical plane of
the rock face, which reveals their width. Note horizontally compressed roots diverging from the axes (arrowheads). Scale bar ¼ 10 mm. DMNH 29594. (E) Rootbearing axes preserved in oblique growth position, with lateral roots compressed along the same plane. Note central stele of axis in the middle, detailed in (F). Scale
bar ¼ 10 mm. HPH 71. (F) Detail of axis and attached root in (E). Note the downward divergence of the root trace preserved in the cortex of the axis (arrow), indicating the direction of growth. Scale bar ¼ 5 mm.
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
Page 11 of 14
FIG. 10. Cottonwood Canyon lycophyte – reconstruction of the rooting system.
Two K-branches diverge from a leafy stem, each of which gives rise to a new
leafy stem and a root-bearing axis. Root-bearing axes bear reduced leaves along
the base and grow into the substrate. Growth orientations differ between the two
root-bearing axes illustrated, consistent with orientations observed in in situ
specimens. Lateral roots diverge horizontally from root-bearing axes and exhibit
variable arrangement along the axes. Scale bar ¼ 20 mm.
Cottonwood Canyon we observe multiple layers of in situ plant
populations, represented by stem mats, which produced rooting
systems that penetrate and are preserved in the underlying
layers (Fig. 9A, B). The highest densities of rooting structures
are seen below the uppermost plant population observed, where
numerous in situ root-bearing axes are exposed in the rock profile (Fig. 9B–D).
The effects on rock texture and structure associated with pedogenic-type interactions of these rooting strucures are not immediately apparent in fresh exposures of the layers containing the in
situ root-bearing axes. However, weathered profiles reveal conspicouous differences between those layers and the sediment below the depth of root penetration (Fig. 9B–D). Together with the
stratigraphic recurrence (Fig. 9) and density of the rooting structures, this demonstrates that substantial plant–substrate interactions were under way by Early Devonian time.
Root gravitropism in lycophytes
The root tufts of the Cottonwood Canyon lycophyte are consistently found spreading along horizontal planes from
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FIG. 9. Outcrop at Cottonwood Canyon. (A) Stratigraphy of layers containing in situ specimens of the Cottonwood Canyon lycophyte. Darker shale layers containing
in situ stem mats (arrows) alternate with lighter, thicker siltstone layers, in which downward-growing root-bearing axes are preserved (see Fig. 8). Hammer
head ¼ 17 cm across. (B) Uppermost stem mat layer (arrow) overlying a thick siltstone layer. The approx. 12-cm-thick zone at the top of this siltstone layer (bracket)
contains numerous vertical in situ root-bearing axes and exhibits much more pronounced oxidation mottling than the layers below, reflecting pedogenic effects of
rooting structures. (C) Detail of rooting zone of siltstone layer in (B) showing exposed oxidized root-bearing axes (arrows) and pronounced oxidation mottling.
Quarter dollar coin is shown for scale. Brackets in (B) and (C) indicate the same thickness of rock. (D) Vertical root-bearing axes in rock specimen originating from
rooting zone in (C). Note bases of diverging roots (arrows). Scale bar ¼ 20 mm. HPH 310.
Page 12 of 14
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
K-branching and lycophyte root evolution
Detailed understanding of lycophyte root evolution is lacking
at present. The early occurrence of lycophyte rooting structures
in the fossil record and the overall diversity of rooting structures within the clade have inspired scenarios of root evolution.
One hypothesis that has been put forth is that lycophyte roots
evolved from K-branches in which one of the arms developed
as a rooting organ and eventually became a root (Gensel and
Berry, 2001; Gensel et al., 2001). The morphology of the
Cottonwood Canyon lycophyte challenges this hypothesis and
suggests an alternative hypothesis for the origin of roots among
lycophytes. In this plant, K-branching does not produce roots
and instead produces a modified stem (the root-bearing axis)
that anchors the plant. It is this modified stem that produces lateral roots, which have no direct developmental relationship
with K-branching. Consequently, the roots of the Cottonwood
Canyon lycophyte show neither serial nor positional homology
with the products of K-branching: roots are not borne on stems
in the position of K-branches, nor are they produced directly by
K-branching in the postion of root-bearing axes, and there are
no other appendages on the root-bearing axes to which the root
tufts could be homologous. These morphological relationships
illustrated by the Cottonwood Canyon lycophyte indicate that
in this plant, and possibly in lycophytes in general, roots are not
derived from K-branches. This suggests strongly that lycophyte
roots may have arisen as a novel organ type.
Early lycophyte rooting systems and the oldest roots
By the end of the Devonian, plant rooting systems were extensive, morphologically complex and taxonomically diverse,
as documented in progymnosperms (Archaeopteris), arborescent lycopsids (Cyclostigma, Protostigmaria, Leptophloeum,
Otzinachsonia) and cladoxylopsids (Eospermatopteris,
Lorophyton, Metacladophyton tetraxylum, Calamophyton)
(Jennings et al., 1983; Fairon-Demaret and Li, 1993; Stewart
and Rothwell, 1993; Weng and Geng, 1997; Algeo and
Scheckler, 1998; Cressler and Pfefferkorn, 2005; Giesen and
Berry, 2013; Prestianni and Gess, 2014). However, comparatively little is known about their Early Devonian precursors,
and in many cases either these early rooting systems or the
plants that produced them are poorly understood.
Lycophyte rooting systems appear much earlier in the fossil
record than those of euphyllophytes, for which the earliest are
known from the Middle Devonian (Calamophyton; Giesen and
Berry, 2013). The earliest lycophyte rooting systems are seen in
Lochkovian–Pragian Zosterophyllum, whose K-branches produce axes with inferred downward growth (Hao et al., 2010).
The rooting structures of Early Devonian lycophytes span a
broad range of morphologies derived from either (1) branches
formed by K-branching or (2) structures comparable to lateral
adventitious roots (e.g. Edwards, 1994; Raven and Edwards,
2001; Gensel et al., 2001; Kenrick, 2002). Rooting structures
derived from K-branching are produced on the simple axes of
Zosterophyllum (Walton, 1964; Hao et al., 2007, 2010),
Bathurstia (Kotyk and Basinger, 2000; Gensel et al., 2001) and
Sawdonia (Rayner, 1983). Leafless axes interpreted as rooting
organs are also produced by K-branching of stems of
Drepanophycus spinaeformis (Gensel et al., 2001) and, possibly, D. devonicus (Schweitzer and Giesen, 1980) and the
Middle Devonian D. minor (Xu et al., 2013). Although such
structures derived from K-branching may have functioned as
rooting organs, they do not represent roots because they are
branches of simple axes or stems, produced by apical
dichotomy.
Lateral organs that, in our opinion, more closely resemble
adventitious roots have been documented from several taxa.
These organs occur as smooth or sinuous lateral axes seen in
Crenaticaulis, Bathurstia and Drepanophycus (Gensel et al.,
2001), or tufts of fine branching axes documented in
Drepanophycus (Schweitzer and Giesen, 1980; Li and
Edwards, 1995; Gensel et al., 2001), Taeniocrada (Schweitzer,
1980), Hsua (Li, 1992) and Crenaticaulis (Gensel et al., 2001).
Asteroxylon mackiei also produced leafless rhizomatous axes
and fine root-like structures with inferred positive gravitropism
(Kidston and Lang, 1920, 1921). The oldest of these Early
Devonian structures are known from the Pragian Bathurstia and
Drepanophycus, reported from Bathurst Island by Kotyk and
Basinger (2000) and Gensel et al. (2001). Although these
Pragian records may represent roots, they have been referred to
tentatively as rooting structures due to the absence of diagnostic
characters such as endogenous origin and a root cap (e.g.
Gensel et al., 2001).
With the exception of Zosterophyllum shengfengense
(Hao et al., 2010), which preserves above-ground axes and attached rooting systems, the overall architecture of the early
rooting systems discussed above is poorly understood. In many
of these plants, rooting structures are seen only on rare specimens and are not preserved in situ. Conversely, the extensive
Emsian rooting system documented by Elick et al. (1998) is
one of few Early Devonian rooting systems preserved in growth
position, but it cannot be attributed unequivocally to a known
taxon. Thus, for these early rooting systems very limited
data are available on their overall structure, morphological
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subtending in situ root-bearing axes, whether the latter are horizontal or vertical. This indicates that the roots may have lacked
a positive gravitropic response, suggesting that in this plant root
identity was developmentally uncoupled from positive gravitropism. Instead, direct evidence for the presence of a gravitropic response is provided by the downward growth
documented in root-bearing axes. Consistent recurrence of
downward orientated in situ axes bearing horizontally spreading
roots in successive plant populations demonstrates that these
growth patterns represent constitutive structural traits and not
opportunistic responses of a flexible developmental
programme.
Furthermore, the origin of these axes as branches of a shoot
system suggests that in lycophytes the positive gravitropic response mechanism evolved first in specialized stems and not in
roots. Bolstering this idea, in some Zosterophyllum species that
lack roots altogether, branching produces axes with inferred
downward growth (Walton, 1964; Gensel et al., 2001; Hao
et al., 2007, 2010), consistent with positive gravitropism. This
raises the possibility that positive gravitropism was not among
the signal transduction programmes of the earliest lycophyte
roots and that it was co-opted as a root developmental pathway
later, within this clade.
Matsunaga and Tomescu — Root evolution: insights from an Early Devonian lycophyte
ACKNOWLEDGEMENTS
We are indebted to Brent Breithaupt, US Bureau of Land
Management Regional Paleontologist, for providing permits
to collect at Cottonwood Canyon. We thank William
DiMichele, Carol Hotton, Nathan Jud and Jonathan Wingerath
(National Museum of Natural History – Smithsonian
Institution); Thomas N. Taylor, Edith L. Taylor and Rudolph
Serbet (University of Kansas); Kirk Johnson and Ian Miller
(Denver Museum of Nature and Science); Ian Glasspool and
Patrick Herendeen (Field Museum of Natural History) for access to collections and specimen loans. We also thank
Christopher Steenbock, Joseph Caruso, Richard Tate, James
Cornwell, Glenn Shelton, Allison Bronson, Ashley Ortiz,
Hannah Barrett-Watson, Jeffery Barrett and Rachel Klassen
for assistance in the field and lab. Peter Holterhoff provided
assistance in the field and helpful information on stratigraphy
and depositional environments. Comments from Gar
Rothwell, Michael Mesler, Terry Henkel and three anonymous
reviewers greatly improved the manuscript. This work was
supported by graduate student research awards from the
Botanical Society of America, Geological Society of America,
Paleontological Society (James M. and Thomas J. M. Schopf
Award), and Humboldt State University Department of
Biological Sciences to K.K.S.M., and by grants from the
Humboldt State University Office of Research and Graduate
Studies, Humboldt State University Sponsored Programs
Foundation, and the American Philosophical Society to
A.M.F.T.
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