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First published online 24 January 2007
doi: 10.1242/dev.001008
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1 Department of Plant Sciences, University of Oxford, South Parks Road, Oxford
OX1 3RB, UK.
2 Systems Biology Laboratory, 127 Milton Park, Abingdon, Oxfordshire OX14 4SA,
UK.
* Author for correspondence (e-mail: jane.langdale{at}plants.ox.ac.uk)
Accepted 2 January 2007
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SUMMARY |
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 TOP SUMMARY INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key words: Meristem function, Leaf development, Lycophytes, Lineage analysis
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INTRODUCTION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). By
contrast, flowering plants branch through the outgrowth of axillary meristems
that are themselves produced in association with leaves by the main SAM.
Distinct leaf morphologies also distinguish these two plant groups in that
lycophytes have microphyllous leaves typically with a single vascular trace,
whereas flowering plants have megaphyllous leaves with complex venation
patterns (Gifford and Foster,
1989; Kenrick and Crane,
1997).
In flowering plants, meristem structure and function is reasonably well
understood. The SAM is both layered and zoned (reviewed by
Steeves and Sussex, 1989).
Cells in the outer L1 layer divide anticlinally to extend the epidermis of the
plant, whereas cells in the subtending L2 and L3 layers divide randomly to
contribute to inner tissues. Zones are superimposed upon layers, with cells of
the central zone both self-renewing and contributing to the flanking
peripheral zone, and cells of the peripheral zone contributing to determinate
lateral organs. Throughout development, these zones and layers are maintained
and meristem size is relatively invariant.
The balance between indeterminate shoot and determinate leaf growth in
flowering plant SAMs is regulated by several interacting pathways. For
example, KNOTTED1-like homeodomain (KNOX) proteins function to promote
indeterminacy in the meristem, whereas ARP-type Myb transcription factors
promote determinacy in leaf primordia by downregulating KNOX
expression (Jackson et al.,
1994; Lincoln et al.,
1994; Long et al.,
1996; Nishimura et al.,
1999; Sentoku et al.,
1999). A failure to downregulate KNOX gene expression in
the leaf can perturb both mediolateral (M-L)
(Scanlon et al., 1996) and
proximodistal (P-D) axis formation
(Lincoln et al., 1994;
Smith et al., 1992;
Tsiantis et al., 1999),
suggesting an interaction between meristem function and axis formation in the
leaf. This link is further substantiated by the observation that class III
HD-Zip genes, such as PHABULOSA (PHB), both promote meristem
activity and confer adaxial leaf fate
(McConnell et al., 2001).
Aspects of both the KNOX-ARP and HD-ZIP pathways function in the lycophyte
Selaginella kraussiana (Floyd and
Bowman, 2006; Floyd et al.,
2006; Harrison et al.,
2005; Prigge and Clarke,
2006). However, the context in which these pathways operate is not
yet clear because our current understanding of lycophyte SAMs is based solely
on histological analyses.
Although anatomical descriptions provide some insight into how meristems
function, interpretations of the data obtained are often conflicting owing to
the limitations of analysing static views of a dynamic process. In the case of
lycophyte meristems, competing hypotheses exist to explain how leaves are
initiated on the flanks of the apex
(Dengler, 1983;
Hagemann, 1980;
Wardlaw, 1957), how many and
how apical initials contribute to shoot growth
(Hagemann, 1980;
Newman, 1965;
Philipson, 1990;
Popham, 1951;
Von Guttenberg, 1966), and how
meristem bifurcation occurs (Hagemann,
1980; Von Guttenberg,
1966). To resolve these issues, we have carried out a clonal
analysis in S. kraussiana. This approach offers a distinct advantage
over histological studies as it elucidates cell lineage relationships in a
three-dimensional context and monitors the fate of individual cells. The
choice of S. kraussiana as a model system reflects the evolutionary
significance of lycophytes as the earliest diverging vascular plant lineage,
recent genome initiatives and published `evo devo' studies with this species
(Floyd and Bowman, 2006;
Floyd et al., 2006;
Harrison et al., 2005). We
show here that leaves are initiated from two adjacent epidermal cells on the
flanks of the SAM, that shoots are primarily derived from the activity of two
apical initials, and that these initials contribute directly to the two new
meristems formed after bifurcation. This work provides a robust framework for
future comparative studies of meristem and leaf development in land
plants.
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MATERIALS AND METHODS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) were
grown from cuttings in soil in a Sanyo MLR-350HT growth chamber with 70%
humidity. After 2 months, plants were irradiated with single doses of 250 kV
X-rays at a dose rate of 2.2 Gy per minute. The X-ray generator was operated
at 14 mA, with 0.5 mm Cu and 1 mm Al added filtration (half value layer=1.32
mm Cu). An open-ended perspex applicator was used to restrict the area of the
beam. Optimal dose determination was as described in the results. Plants were
examined for sectors at weekly intervals after irradiation. Small leaf sectors
typically became apparent about 1 month after irradiation, whereas sectors
affecting the shoot became apparent after 2-3 months. Sectored leaves and
shoots were removed from the plant and examined using a Nikon SMZ800
dissecting microscope. Sector position and extent were determined using an
eyepiece graticule and recorded both by photography and by hand on a
line-drawn leaf or shoot template.
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Calculation of apparent cell number (ACN)
Estimates of the ACN at the time of irradiation were obtained using the
reciprocal of the proportion of the sectored part. Thus, where a sector
occupied half of a plant part, one or two cells contributed to that part at
the time of irradiation, depending on whether the cell(s) was in the G1 or G2
phase of the cell cycle [for further discussion see Poethig
(Poethig, 1987)]. On this
basis, if many plants are irradiated at different stages of development,
individual sector types gain multiple representations in the data set and can
be used to reconstruct patterns of cell division.
Histology and cell counts
Segments of fully expanded stem were fixed in 4% paraformaldehyde with 4%
DMSO in PBS, and then dehydrated and embedded in wax or Technovit 7100 resin
as described in the manufacturer's manual (Kulzer). Sections of 3 µm or 10
µm were cut and stained either with 0.1% aqueous Toluidine Blue for 30
seconds, rinsed in water and dried for storage and further examination, or
with Safranin O and Fast Green as previously described
(Berlyn and Miksche, 1976).
Median longitudinal leaf sections were identified using three markers: the
ligule, guard cell files and the leaf vein. Transverse section cell numbers
were counted at the widest point in the leaf. Epidermal and inner
photosynthetic cell layer counts were obtained from stem tissue in
longitudinal and transverse planes. The final numbers presented are averages
of 25 counts. Sections were examined and photographed using a Leica DMRB
microscope.
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RESULTS |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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). To
determine whether sectorial aneuploidy could be induced in heterozygous
au mutants, plants were irradiated with X-rays. Irradiation led to
the formation of white or dark-green sectors following presumed loss of the
wild-type or mutant allele, respectively
(Fig. 1A). Sectors were induced
in all mutant plants irradiated at 25 Gy or more. No sectors were induced in
nonirradiated controls, and few sectors were induced in irradiated wild-type
plants (data not shown). To determine the dose at which the maximum number of
sectors could be induced without deleteriously affecting plant growth,
8-week-old cuttings of both wild-type and mutant plants were irradiated with 0
to 100 Gy, at 25 Gy intervals. In both wild-type and mutant plants, overall
growth was retarded following irradiation doses of 75 Gy or 100 Gy
(Fig. 1B); phenotypic
perturbations such as leaf splitting, change in leaf shape and termination of
the meristem were also observed (Fig.
1C). The optimal dose for sector induction was therefore
determined by irradiating new cuttings at 10 Gy intervals between 30 and 70
Gy. These experiments demonstrated that 40 Gy irradiation induced sectorial
aneuploidy in S. kraussiana au mutant shoots at a sufficient
frequency for clonal analysis without concomitant perturbation to growth
patterns.
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). To determine
the cell autonomy of dark-green and white sectors on heterozygous
au/+ shoots, we searched for single cell sectors. The position and
extent of sectors within leaves was determined using chlorophyll
autofluorescence as a marker of au activity. Chloroplasts fluoresce
dark red in wild-type +/+ or aneuploid +/-cells, pale red in heterozygous
au/+ cells and do not fluoresce in homozygous au/au or
aneuploid au/- cells. Single-cell, dark-red
(Fig. 1D,E) and non-fluorescent
(Fig. 1F,G) sectors were
identified in both the epidermal (Fig.
1E,G) and mesophyll (Fig.
1D,F) layers of the leaf, indicating that the au gene
product acts cell autonomously. As such, au/- and +/-sectors could
reliably be used to elucidate cell lineage relationships in S.
kraussiana.
Leaves are initiated from a pair of cells on the flank of the S. kraussiana SAM
To assess cell lineage relationships within the leaf and to determine how
leaves are initiated in the SAM, 1362 within-leaf sectors were examined.
S. kraussiana leaves are arranged in ranks along a creeping
dorsiventral axis, such that the small leaves are dorsal with the abaxial side
facing upwards, and the larger leaves are ventral with the adaxial side facing
upwards (Fig. 2A). Within each
leaf there are three cell layers: the adaxial epidermis, the mesophyll and the
abaxial epidermis. Sectors were scored by measuring the proportion of leaf
length encompassed, the proportion of leaf width encompassed, and by assessing
chlorophyll fluorescence in each of the three leaf layers
(Fig. 2B and
Table 1).
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Full-length leaf sectors that are one-sixth or one-eighth of the leaf width and extend through two of the three leaf layers suggest the subsequent establishment of the Ad-Ab axis by a symmetrical and downwards division (Fig. 3E,G). The resultant leaf founder-cell population for each type of leaf is therefore a group of twelve or sixteen epidermal cells. As sectors that mark only one Ad-Ab leaf layer extend from one-half to one-sixteenth leaf length (Fig. 3F,G), 1-15 cell divisions must occur in the P-D direction prior to formation of the internal mesophyll layer. Subsequent rounds of cell division give rise to dorsal leaves of 31±5.6 (M-L) x 3 (Ad-Ab) x 45±12.2 (P-D) cells and ventral leaves of 62±7 (M-L) x 3 (Ad-Ab) x 133±10.7 (P-D) cells at maturity.
S. kraussiana shoots have four axes of symmetry
To ascertain the anatomical context in which to assess lineage
relationships within the S. kraussiana SAM, general growth patterns
were first documented. Following germination, and a short period of juvenile
growth where leaves are initiated in spiral phyllotaxy, S. kraussiana
SAMs branch to form two new growth axes - a thicker major stem and a more
slender minor stem (Fig. 4A).
Each stem is flattened dorsiventrally and is ellipsoid in transverse section,
such that stems have both left-right and dorsiventral planes of symmetry. On
each stem, diagonal and intersecting axes mark the position of leaf
initiation, and six or eight opposite and decussate leaf pairs are produced
before each SAM bifurcates again. New axes form on alternate sides of the
shoot at successive branch points giving the shoot a characteristic zig-zag
growth pattern. Stem growth, leaf formation and branching therefore require
the establishment and maintenance of a dorsiventral, two-diagonal and a
left-right axis of symmetry within the shoot
(Fig. 4B).
Shoots that are not bifurcating derive from the four distal-most cells in the SAM
To understand how cell division patterns might establish symmetry in the
S. kraussiana SAM, transverse sections of shoot apices were examined
by light microscopy. Sections cut across the top of the apex showed four
large, lightly staining cells (Fig.
4C,G). The inner two divide in parallel to the left-right axis to
establish dorsiventrality in subtending cell layers, whereas the two lateral
cells divide radially to establish the diagonal axes of symmetry
(Fig. 4D,E,H,I). Leaves arise
around five cell layers below the tip, at the boundary between daughter cells
of an inner and an outer distal-most cell of the four apical cells
(Fig. 4F,J). Left-right,
dorsiventral and diagonal growth axes are therefore established within the top
five cell layers of the meristem, and the two cells that initiate each leaf
are descendants of two different surface cells.
To assess the functional significance of the deduced cell division
patterns, lineage relationships in the SAM were determined by examining
sectors that contributed to all or part of the shoot. No cylindrical sectors
or sectors that occupied the medial third of the shoot were detected,
suggesting the absence of a single apical initial. Half-shoot sectors
typically affected the dorsal and ventral leaf rank on the left or right side
of the stem, as opposed to either the dorsal or ventral leaf ranks
(Fig. 4K). One-quarter-shoot
sectors similarly affected the left or right side of the stem. However, these
sectors were only observed in the left or right lateral quarters and were
never observed in the dorsal and ventral medial quarters
(Fig. 4L). This observation
suggests that left-right shoot symmetry is the first to be established in the
SAM and demonstrates that the inner two distal-most cells divide both to
self-renew and to give rise to the two lateral cells. This capacity for
self-renewal identifies the inner two distal-most cells as apical initials,
and thus the two lateral cells are daughters of initials, i.e. merophytes
(Lyndon, 1990). Sectors on the
dorsal or ventral side of the stem occupied either medial or lateral parts of
the shoot, with a maximum girth of about one-tenth
(Fig. 4M). Consistent with
deduced cell division patterns (Fig.
4H), these sectors must have arisen in one of the eight dorsal or
ventral descendants of the four distal-most cells. In combination, these data
suggest that a strip of four cells on the surface of the SAM gives rise to
most of the shoot. The two inner initials divide both in the left-right axis
to produce the two lateral merophytes (Fig.
4G), and alternately in the dorsal and ventral planes to yield a
further two pairs of merophytes in the subtending cell layer
(Fig. 4H). The lateral
merophytes contribute to growth at each side of the shoot, whereas the
subtending merophytes give rise to the dorsal and ventral sides of the
shoot.
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Apical initial number varies during shoot development
Having established the cell division patterns in the SAM during growth of
an individual minor or major stem, we then assessed what happens in the SAM
when two new stems are formed. To determine the cellular context within which
bifurcation occurs, longitudinal sections of bifurcating apices were examined.
Frontal longitudinal sections of recently bifurcated shoots show four or five
lightly stained large cells in each SAM
(Fig. 6A,E,F). After the SAM
has initiated three leaf pairs, division and lateral expansion yields an
increase in the number of these cells to around six, and a broadening of the
apex (Fig. 6B). After the
initiation of four leaf pairs on the major axis or three leaf pairs on the
minor axis, further asymmetric divisions increase the cell number to seven or
eight (Fig. 6C). When the apex
shows visible signs of bifurcation, there are around 11-13 large cells
(Fig. 6D). Of these, the four
centrally located cells appear to become determinate whereas the two lateral
groups of three or four appear to constitute the large distal cells of the new
major and minor SAMs (Fig.
6E,F).
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DISCUSSION |
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TOPSUMMARYINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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; Philipson,
1990; Popham,
1951). The simplest type is the monoplex meristem that is capped
by a single tetrahedral apical initial that cleaves spirally to contribute to
stem growth (Newman, 1965),
whereas the most complex are arranged into distinct zones and layers with
specialised function. Monoplex meristems are reportedly found in mosses and
ferns, and complex meristems are found in seed plants. Lycophyte meristems are
intermediate between these types but are typically placed at the `simple' end
of the scale. Historically, the concept of monoplex apices has been linked to
the notion of a slowly dividing persistent apical cell
(Newman, 1965). By contrast,
complex meristems of seed plants have a small number of impermanent apical
initials in each layer (Bossinger et al.,
1992; Dulieu, 1969;
Furner and Pumfrey, 1992;
Irish and Sussex, 1992;
Jegla and Sussex, 1989;
Korn, 2001;
McDaniel and Poethig, 1988).
Our data clearly show that apical initials in the S. kraussiana apex
are impermanent and thus it is reasonable to propose that mechanisms that
regulate initial cell activity may be conserved in vascular plants. The data presented elucidate three novel aspects of SAM function during the adult phase of vegetative growth in the lycophyte S. kraussiana. First, two apical initials cleave to give rise to six merophyte daughters that form distinct lateral, dorsal and ventral domains in the stem.
This observation implies a shoot-patterning role for the division sequence of the apical initials. Second, both left- and right-half shoot sectors can take over the whole shoot. Thus, the two apical initials are developmentally equivalent. Third, leaves initiate from two cells, one of which is derived from a medial merophyte, and one from a lateral merophyte. This suggests that apical cell symmetry may also pattern the M-L leaf axis. The presence of two apical initials thus provides a capacity for regulating shoot symmetry that does not exist in apices with a single apical initial. This illustrates that a seemingly simple transition from a spirally cleaving apical initial to a pair of side-by-side developmentally equivalent initials can generate radical alterations in plant form.
A conspicuous difference in growth form between S. kraussiana and
flowering plants results from their different modes of branching. In
lycophytes, branching is attained by bifurcation of the meristem, whereas in
flowering plants vegetative branches form in the leaf axils. Although it was
initially proposed that axillary meristems resulted from the activity of
`detached' meristem remnants in the leaf axil
(Garrison, 1955), more recent
work has shown that, at least in eudicots, axillary meristems form from the
adaxial leaf surface (McConnell and
Barton, 1998). Axillary meristems may be clonally related to the
subtending leaf and internode as in Arabidopsis thaliana
(Furner and Pumfrey, 1992;
Irish and Sussex, 1992), or to
the internode and leaf above as in maize
(Johri and Coe, 1983;
McDaniel and Poethig, 1988).
Previous histological studies of Selaginella have similarly disputed
whether apical initials contribute directly
(Hagemann, 1980) or indirectly
(Von Guttenberg, 1966) to
branch meristem formation. In contrast to the mode of establishment of
axillary meristems, and to suggestions from histological studies, we conclude
that initials in both the major and minor branch SAMs are direct descendants
of those in the parent SAM. This observation negates the need to invoke de
novo initial specification during bifurcation, and highlights an important
distinction between bifurcation and axillary branching.
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), which
suggests that megaphylls arose by overtopping, planation and webbing of
subsets of shoots within a dichotomously branched shoot system
(Kenrick, 2002;
Zimmermann, 1952). As yet, few
mechanisms have been proposed to explain how these processes may have
operated. In S. kraussiana, the bifurcating shoot system is unequal,
with one branch overtopping the other and becoming the major axis. Within the
context of the telome theory, the minor branch of the S. kraussiana
shoot is therefore equivalent to a `proto' megaphyll. The data presented here
suggest that these inequalities in shoot growth result from differences in the
number of apical initials inherited by daughter branches: major branches
initiate growth from two apical initials, whereas minor branches originate
from just one. Thus, overtopping, and hence megaphyll evolution, may have
arisen from a simple mechanism whereby apical cell partitioning during
branching resulted in fewer apical initials and reduced growth in side
branches, relative to main branches.
Leaf initiation and axis formation
The data presented here demonstrate that the leaves of S.
kraussiana initiate from two adjacent epidermal cells. These two cells
first divide to extend the M-L axis, then to initiate the Ad-Ab axis and
finally to establish the P-D axis, yielding a founder population of twelve or
sixteen epidermal cells. One conspicuous distinction between S.
kraussiana and seed plant leaves is therefore the number of founder cells
recruited to form the primordium. In all seed plants in which clonal analyses
have been performed, the number of leaf founder cells ranges from 100-200
(Dolan and Poethig, 1998;
Korn, 2002;
Poethig, 1984;
Poethig and Szymkowiak, 1995).
The 12-16 leaf founder cells in S. kraussiana are therefore more
comparable to the number recruited to form floral organs in
Arabidopsis (Bossinger and Smyth,
1996). This similarity may reflect the relatively small size of
the S. kraussiana SAM and Arabidopsis floral meristems.
A further difference between S. kraussiana and seed plant leaves
is seen in the order of axis development within the organ. The pattern deduced
here for S. kraussiana differs from that previously suggested from
histological analyses where the Ad-Ab axis
(Wardlaw, 1957) or the P-D
axis (Dengler, 1983) was
thought to be established first. Interestingly, the pattern of S.
kraussiana leaf initiation inferred here is strikingly similar to moss
and liverwort gametophyte leaf development, where one and then two
side-by-side cells undergo M-L and P-D divisions to give rise to a leaf with a
single cell layer (Janzen,
1929). Fern scales reportedly form in the same way
(Bower, 1935). The main
developmental difference between moss gametophyte leaves, fern scales and
S. kraussiana leaves, however, is the capacity of leaf founder cells
in S. kraussiana to divide in a third plane that initiates the Ad-Ab
axis, and then ultimately gives rise to the inner leaf layer
(Dengler, 1983). Notably, in
seed plant leaves the Ad-Ab layers are patterned from inception because leaf
founder cells are recruited from both epidermal and sub-epidermal layers of
the meristem. Thus, key differences between microphylls of S.
kraussiana and megaphylls of seed plants are the number of meristematic
cell layers recruited into the primordium and the consequent mode of axis
establishment.
Theories of microphyll evolution
Because the lycophyte leaf cannot be easily interpreted in terms of the
telome theory, three further theories have been advocated to explain their
origin (Kenrick, 2002). The
reduction theory suggests that lycophyte leaves were derived by reduction of
flattened lateral branches or megaphylls
(Zimmermann, 1959), whereas
the enation theory states that leaves arose spontaneously from the stem as
epidermal outgrowths (Bower,
1908), and the sterilisation theory suggests that leaves are
modified sporangia (Crane and Kenrick,
1997; Kenrick,
2002; Kenrick and Crane,
1997). From a developmental perspective, the reduction theory
implies a switch from indeterminate to determinate growth in a lateral branch,
whereas the enation theory invokes the de novo introduction of a determinate
developmental pathway in stem epidermal tissue, and the sterilisation theory
implies a switch in branch fate within the context of an already determinate
lateral organ (Kenrick,
2002).
Recent developmental studies have attempted to resolve which of the three
theories of lycophyte leaf evolution is most plausible by examining expression
patterns of genes that are orthologous to those involved in megaphyll
development. KNOX and ARP gene expression patterns in the
S. kraussiana apex support the reduction theory in that concomitant
KNOX gene downregulation and ARP gene upregulation occurs in
leaves of both microphyllous and megaphyllous species
(Harrison et al., 2005).
However, this observation may simply reflect the fact that both microphylls
and megaphylls are determinate structures, and the KNOX-ARP interaction can be
interpreted as regulating indeterminacy versus determinacy. Support for the
enation theory has been argued from analysis of S. kraussiana HD-Zip
gene expression patterns (Floyd and
Bowman, 2006). There are two HD-Zip genes in S.
kraussiana, one of which is expressed in the leaf and one in the stem
vasculature (Floyd and Bowman,
2006; Floyd et al.,
2006; Prigge and Clarke,
2006). Since the gymnosperm orthologue of the Selaginella
`stem vasculature' gene is expressed in both the leaves and stems of
representative seed plants, the authors favour the hypothesis that microphylls
and megaphylls evolved through co-option of distinct developmental mechanisms,
or at least distinct HD-Zip gene functions
(Floyd and Bowman, 2006).
However, this inference assumes that both gene paralogues have retained the
function that they originally performed in the lineage that gave rise to
S. kraussiana, yet there are many examples of paralogues switching
function in other systems (Wray and
Abouheif, 1998). With respect to the sterilisation theory, the
genetic basis of sporangial development is unexplored. However, sporangia in
leptosporangiate ferns initiate from single superficial cells in a manner
reminiscent of leaf initiation in S. kraussiana
(Gifford and Foster, 1989). It
therefore remains a possibility that mechanistic support for the sterilisation
theory may be forthcoming in the future. In combination, these observations
suggest that despite the recent elucidation of aspects of leaf development in
S. kraussiana (Floyd and Bowman,
2006; Harrison et al.,
2005; Prigge and Clarke,
2006), the data obtained do not allow distinction between the
existing theories of lycophyte leaf evolution. It might therefore be more
beneficial to determine what distinguishes bifurcating shoot systems and
megaphylls from epidermal protrusions such as lycophyte microphylls, moss
gametophyte leaves and fern scales.
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ACKNOWLEDGMENTS |
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