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Anatomy and Morphology |
Department of Chemical and Biological Sciences, Japan Women's University, 8-1, Mejirodai 2-chome, Tokyo 112-8681 Japan; Division of Biology, Department of Natural Science, Jikei University, School of Medicine, 3-1, Kokuryo 8-chome, Chofu, Tokyo 182-8570, Japan
Received for publication November 6, 2006. Accepted for publication October 8, 2007.
ABSTRACT
Vascular plants have evolved shoot apical meristems (SAMs), whose structures differ among plant groups. To clarify the evolutionary course of the different structural types of SAMs, we compared plasmodesmatal networks in the SAMs for 17 families and 24 species of angiosperms, gymnosperms, and pteridophytes, using transmission electron microscopy (TEM). The plasmodesmata (PD) in almost all cell walls in median longitudinal sections of SAMs were counted, and the PD density per unit area was calculated for each cell wall. Angiosperm and gymnosperm SAMs have low densities, with no difference between stratified (tunica-corpus) and unstratified structures. SAMs of ferns, including Psilotum and Equisetum, have average densities that are more than three times higher than those of seed plants. Interestingly, microphyllous lycopods have both the fern and seed-plant types of PD networks; Selaginellaceae SAMs with single apical cells have high PD densities, while SAMs of Lycopodiaceae and Isoetaceae with plural initial cells have low PD densities, equivalent to those of seed plants. In summary, PD networks are strongly correlated to SAM organizations—SAMs with single and plural initial cells have the fern and seed-plant types of PD, respectively. The two SAM organizations may have evolved separately in lycophytes and euphyllophytes and may be associated with gain or loss of the ability to form secondary PD.
Key Words: ferns • lycopods • monilophytes • plasmodesmata • seed plants • shoot apical meristem • vascular plants
The body of vascular plants is generated by indeterminate activities of the shoot and root apical meristems. Shoot apical meristems (SAMs) are generally believed to have evolved independently in lycophytes, ferns, and seed plants in association with establishment of the stem and leaf (e.g., Kenrick and Crane, 1997
; Friedman et al., 2004
). SAMs of vascular plants have a wide variety of structure (Clowes, 1961
; Buvat, 1989
; Gifford and Foster, 1989
; Steeves and Sussex, 1989
; Lyndon, 1998
). Ferns (monilophytes, sensu Pryer et al., 2004
) have a single initial cell called the apical cell that produces all SAM constituent cells as shown by the elegant work of Bierhorst (1977)
. In contrast, SAMs of gymnosperms and angiosperms have no apparent single apical cell. Gymnosperm SAMs have zonal patterns (e.g., Foster, 1938
, 1939
, 1941
). For example, Ginkgo SAMs have five zones: the apical initial group, central mother cells, the transition zone, the peripheral subsurface layer of cells, and the rib meristem (Foster, 1938
). Angiosperm SAMs have a stratified structure composed of the tunica, which comprises surface and subsurface layers, and the corpus, which comprises the underlying mass of cells (Schmidt, 1924
). Lycophyte SAMs have either an apical cell or plural apical initials (Gifford and Foster, 1989
).
Irrespective of structural differences in SAMs among vascular plants, some authors find advantages in describing SAMs of not only gymnosperms and angiosperms but also of ferns using the zone concept (Stevenson, 1976
; Gifford, 1983
; Steeves and Sussex, 1989
). In this concept, the apical cell or cells are not distinguished from other adjacent cells in the initiating region of a SAM (McAlpin and White, 1974
; Gifford, 1983
). Recent gene expression analyses have provided insights into the cytohistological zonation of angiosperm SAMs (Nishimura et al., 1999
; Fletcher and Meyerowitz, 2000
). Furthermore, KNOX genes required for maintaining SAMs are expressed similarly in angiosperm SAMs and SAMs of megaphyllous ferns and microphyllous lycophytes (Harrison et al., 2005
; Sano et al., 2005
). Taken together, these data raise questions—if the SAMs of all vascular plants are considered functionally identical, what does the difference in structure purport?
Gymnosperm and angiosperm SAMs are believed to have one to three founder (initial) cells in each of the apical layers (Stewart and Dermen, 1970
). Therefore, SAMs evidently have either single or plural initial cells, depending on the plant group (Philipson, 1990
). A balanced population of initial cells is maintained by an autoregulatory feedback loop between the WUS and CLV genes in the model angiosperm plant, Arabidopsis thaliana (Mayer et al., 1998
; Carles and Fletcher, 2003
; Veit, 2006
). It remains an open question whether the initial cell population is regulated similarly in gymnosperm and fern SAMs. If the difference in initial cell number correlates to different SAM structures, then is there an underlying mechanism causing this association?
The coordinated growth of the plant body requires some kind of cell-to-cell signaling, perhaps via trafficking of regulatory proteins and/or mRNAs (Mezitt and Lucas, 1996
; Fosket, 2002
; Foster et al., 2002
; Haywood et al., 2002
; Heinlein, 2002
; Ding et al., 2003
). Such trafficking is via plasmodesmata (PD), cylindrical tubes that are associated with the endoplasmic reticulum (desmotubules) in adjoining cell walls (Robards and Lucas, 1990
; Van der Schoot and Rinne, 1999a
; Roberts, 2005
; Carraro et al., 2006
). Previous studies show that the PD of vascular plants originated from the common ancestors of Chara (a sister of land plants) and land plants (Lucas et al., 1993
; Cook et al., 1997
). Therefore, it seems likely that PD in bryophytes and all vascular plants are comparable or homologous (Cook and Graham, 1999
; Raven, 2005
). The few recent publications on PD networks in SAMs indicate that the frequencies of PD in walls differ between ferns and angiosperms (Robards, 1976
; Cooke et al., 1996
). Ferns develop lineage-specific networks of primary PD (LPD), which are formed in expanding cell plates during cytokinesis. In contrast, angiosperms develop interface-specific networks of both primary and secondary PD (IPD); the secondary PD are inserted into pre-existing walls (Jones, 1976
; Ehlers and Kollmann, 2001
). From the available data, SAM structures may correlate with networks of PD. Because data on these networks are very fragmentary, in this study we compared the networks of PD in vascular plants with different SAM organizations, i.e., microphyllous and megaphyllous pteridophytes, gymnosperms, and angiosperms. We then discuss the evolution of SAM structures in vascular plants based on our results.
MATERIALS AND METHODS
Plant materials
SAMs of 17 families and 24 species of angiosperms, gymnosperms, euphyllous ferns (monilophytes, sensu Pryer et al., 2004
), and microphyllous lycopods were examined (Table 1). One species each of primitive angiosperms (Amborella trichopoda); asterids (eudicots, Aucuba japonica); rosids (eudicots, Arabidopsis thaliana); and monocots (Tradescantia fluminensis), was used as representative angiosperms. Five genera and five species were chosen from all four clades of gymnosperms (Cycadales, Ginkgoales, Coniferales, and Gnetales). Six species of Psilotum (whisk ferns), Equisetum (horsetails), Angiopteris (marattioid ferns), Osmunda (osmundaceous ferns), and Hypolepis (leptosporangiate ferns) were examined for ferns. Nine species of Isoetes, Huperzia, Lycopodiella, Lycopodium, and Selaginella were chosen as representatives of lycopods.
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Shoot tips from two and three independent plants (single SAM/plant) were examined for Aucuba japonica, Tradescantia fluminensis, Hypolepis punctata, and Selaginella martensii, and Amborella trichopoda and Lycopodium clavatum, respectively (Table 1). For Gnetum gnemon, three shoot tips were collected from the same plant. For the rest of the species, a single shoot tip per plant was examined as the representative of each plant SAM.
Transmission electron microscopy
Semicylindrical pieces (less than 1.5 mm thick) of the shoot tip including the SAM were cut off under a binocular dissecting microscope. Samples were fixed overnight in 2.5% glutalaldehyde (GA) in 0.1 M phosphate buffer (pH 6.8) at 4°C, rinsed three times in 0.1 M phosphate buffer (pH 6.8), and then postfixed with 2% osmium tetroxide in 0.1 M phosphate buffer for 1 h at 4°C. Under the same protocol, Isoetes asiatica and I. japonica were fixed with 0.5% GA, and I. pseudojaponica was fixed with 0.25% GA. All fixed materials were dehydrated in an ethanol–acetone series and embedded in epoxy resin (Quetol-653 resin, Nisshin EM, Tokyo) at 60°C for 48 h. Ultrathin sections of about 80 nm were cut on a Reichert OmU3 ultramicrotome (Leica, Vienna), stained with uranyl acetate and lead citrate, and observed with an H-7000 transmission electron microscope (Hitachi, Tokyo).
Plasmodesmata
PD were counted on montages of electron micrographs of median longitudinal sections of shoot tips (Fig. 1A–D) in transversely sectioned cell walls, i.e., with plasmodesmata sectioned longitudinally (Fig. 1C, left cell wall). PD in obliquely or paradermally sectioned walls (Fig. 1C, right cell wall) were not counted, nor were PD in walls of cells that were highly plasmolyzed.
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Calculation of PD densities
PD numbers for each cell wall were calculated per 1 µm of cell wall length. These PD numbers were equivalent to PD numbers in a narrow rectangular area of cell wall 1000 nm long x 80 nm wide (section thickness in present examination). Therefore, for estimating PD frequency per 1 µm2 of cell wall, PD numbers per 1 µm could be multiplied by 1000/80. However, this simple calculation is an overestimate because a single plasmdesma might be double-counted in two serial sections if part of the PD radius is in one section and the rest is in the neighboring section (Robards, 1976
). To limit overestimation of PD numbers per 1 µm cell wall length, we used Gunning's (1978) proportionality constant, 1000/T + 1.5R, where T = section thickness and R = radius of PD. The radius was calculated from the average PD diameter, measured in the middle portion of the cross section. Ten PD were arbitrarily chosen in a sectioned cell wall and measured. In case of multiple SAM observations, R values obtained from a certain single SAM were used for the PD density calculation for other SAMs. In the present examination, T is 80 nm, and R differs with species. For example, in a cell wall of Hypolepis punctata, the PD number per 1 µm (1000 nm) length was 6.46, PD radius was 16.6 nm, and the estimated PD number per 1 µm2 was 6.46 x [1000/(80 + 16.6 x 1.5)] = 61.6.
Determining the exact boundary for the SAM in longitudinal sections of the shoot tip to draw on the micrographs was not easy, so the area above the insertion site of the youngest leaf primordium was regarded as the SAM zone (Figs. 2–5). PD densities were averaged for almost all cell walls of a SAM zone in its median longitudinal section and referred to as "average PD density." PD densities were also averaged for only anticlinal walls of the apical cell and adjacent surface cells (for ferns and Selaginella) or apical initials and their closest neighboring surface cells (for seed plants and Lycopodiaceae and Isoetaceae) and referred to as average PD density of SAM summit. These two data sets of average PD density were obtained for two or three shoot tips of Amborella trichopoda, Aucuba japonica, Tradescantia fluminensis, Gnetum gnemon, Hypolepis punctata, Lycopodium clavatum, and Selaginella martensii, as mentioned earlier. The average PD densities varied among the shoot tips in a species, but the range was not large. Therefore, for the other species, one selected shoot tip was used for the PD count and calculation.
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RESULTS
Two types of PD networks
The PD diameters ranged from 26 to 45 nm with no clear distinction between plant groups (Table 1). PD numbers per unit area of cell wall (PD/µm2) varied among SAMs within species. The maximum and average PD densities from multiple SAMs from some selected species (Amborella trichopoda, Aucuba japonica, Tradescantia fluminensis, Gnetum gnemon, Hypolepis punctata, Lycopodium clavatum, Selaginella martensii) differed among individual SAMs (Table 1). The range of individual differences for those species was 1.1 times (12.3/11.3 for T. fluminensis) to 2.6 times (9.3/3.6 for Amborella trichomoda) in the maximum PD density, and the average PD density differed by 1.0 times (3.4/3.3 for L. clavatum) to 2.3 times (3.7/1.6 for A. trichopoda) in the average PD density. On the other hand, the minimum PD density differed little (Table 1). Many walls had 0 PD/µm2, but this absence does not mean that the entire cell wall lacked PD—it only indicates that PD were not found in the observed sections.
Although the maximum PD density in a SAM differed within species (e.g., 3.6–9.3 PD/µm2 for Amborella trichopoda; Table 1) mentioned earlier, the range of differences was greater between plant species than within species. For example, the SAM of Huperzia serrata had 3.4 PD/µm2 while the SAM of Hypolepis punctata had 113.9 PD/µm2 (Table 1). The lack of SAMs with maximum PD densities between 14.3 (Gnetum gnemon) and 56.1/µm2 (Selaginella limbata) indicates two distinct SAM groups: one with maximum PD densities ranging from 3.4 to 14.3/µm2 and the other with maximum densities from 56.1 to 113.9/µm2. These same two groups of species also differed significantly (permutation test, P < 0.001) in average PD densities for cell walls of a whole SAM (average PD density ranges for the two groups were 0.4–6.2/µm2 and 19.0–56.5/µm2, respectively; Table 1).
The group with low maximum PD densities (3.4–14.3/µm2) and low average PD densities (0.4–6.2/µm2) includes angiosperms, gymnosperms, and some homosporous and heterosporous lycopods; the group with high maximum PD densities (56.1–113.9/µm2) and high average PD densities (19.0–56.5/µm2) includes Angiopteris, Hypolepis, Osmunda (megaphyllous ferns), Psilotum (whisk ferns), Equisetum (horsetails), and Selaginella (heterosporous lycopods). The minimum PD density in a SAM was 0 for most examined species (Table 1), but the frequency of cell walls with 0/µm2 in SAM was much lower in ferns and Selaginella than in seed plants, Lycopodium, and Isoetes (Figs. 2–5).
Seed plants
PD densities in periclinal and anticlinal walls of the surface tunica (L1), subsurface tunica or corpus (L2), and underlying cell (L3) layers of angiosperm SAMs were almost equal, i.e., there was no gradient in PD density from surface cells to the rib meristem (Fig. 2A, B). In gymnosperm SAMs, there seemed to be no difference in PD densities between the central mother cells and peripheral cells in species with no apparent L1 layer, including Ginkgo (Fig. 2C), Cycas, and Pinus (data not shown), and in species with an apparent L1 layer (tunica-like surface layer, Gifford, 1943
), including Gnetum (Fig. 2D) and Ephedra (data not shown). Average PD densities for anticlinal walls of apical initials and their closest neighboring cells (average PD density for SAM summit) were almost equal to the average of all cells in a whole SAM (average PD density) in angiosperm and gymnosperm SAMs (Table 1), suggesting that there is no apparent gradient or regional difference in PD density within whole SAMs. In conclusion, there is no difference in PD density between gymnosperms and angiosperms.
Ferns (monilophytes)
The average PD densities of SAMs of Hypolepis punctata (Fig. 3A), Equisetum species (Fig. 3C), and Psilotum nudum (Fig. 3D–F), all of which have an apparent apical cell with three cutting faces, were more than three times higher than those of angiosperms and gymnosperms (Table 1). The lateral walls of apical cells had high PD densities in a whole SAM, but they were not always the highest. Sometimes, the highest PD densities were in the periclinal or anticlinal walls of cells near the apical cell. SAMs of Osmunda japonica (Fig. 3B) and Angiopteris lygodiifolia (Table 1), whose apical cells were not distinguishable in a longitudinal section in the present examination, also had higher PD densities in apical portions.
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). Like fern gametophytes, SAMs of Hypolepis and Psilotum had decreasing PD densities from the first to third lateral walls (Fig. 3A, D, F). It was hard to detect a trend toward further decreasing PD densities in older original lateral walls in longitudinal sectional views because of the three-dimensional structure of the sporophyte SAM. Periclinal walls near the apical cells or adjacent derivatives often had high PD densities. In fern SAMs, the average PD densities were always lower for the whole SAM than for SAM summit (Table 1). This result is consistent with the fact that the original lateral walls of the apical cell had the highest PD densities, as mentioned earlier.
Lycopods
Two clear PD distributions (seed-plant type and fern type) were found in the lycopods. Lycopodiella (Table 1), Huperzia (Fig. 4C), and Lycopodium (Fig. 4D) had low average PD densities in the entire SAM with plural initials. Isoetes SAMs with prominent initial cells on the surface also had low average PD densities (Fig. 4A, B). In contrast, Selaginella SAMs, which have single apical cells, had fern-type PD networks with much higher average PD densities than Lycopodiaceae SAMs (Fig. 5A, B). Selaginella SAMs were like fern SAMs in that the last-formed lateral walls of the apical cell had the highest PD densities, with decreasing PD densities in older original lateral walls (Fig. 5A).
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Plasmodesmatal networks and SAM organizations
Comparison between 17 families and 24 species of vascular plants showed two distinct types of SAM: fern type with high mean PD densities, and seed-plant type with low mean PD densities. The fern-type PD densities were more than three times those of the seed-plant type. The data were consistent with those of other authors for cell walls of angiosperm SAMs (Glechoma, Chenopodium, and Lycopersicon) and fern SAMs (Pteris and Osmunda) (Cooke et al., 1996
). This distinctive difference was strongly supported by our statistical permutation test.
The fern and seed-plant types are equivalent to the lineage-specific network (LPD) and interface-specific network (IPD), respectively, proposed by Cooke et al. (1996)
for ferns and angiosperms. Hereafter, we refer to the fern type of PD networks as LPD and to the seed-plant type of PD networks as IPD. The IPD SAM is present in gymnosperms and angiosperms, while the LPD SAM is present in monilophytes (sensu Pryer et al., 2004
), including whisk ferns, marattioid ferns, horsetails, and leptosporangiate ferns. Contrary to the general idea that pteridophytes have the LPD SAM, microphyllous lycopods have both LPD and IPD; Selaginella has the LPD SAM (like ferns), and Lycopodium and Isoetes have the IPD SAM (like seed plants).
There have been many attempts to produce workable classifications of SAM types, based mainly on the number and positions of initial cells. Popham (1951
, 1960
) proposed five types; Newman (1965)
reduced this five to three, and Philipson (1990) reduced those three to two. Newman's (1965) three types have been widely accepted; the apical-cell-based SAM of ferns is called monoplex, the gymnosperm SAM with plural initial cells in one zone is called simplex, and the angiosperm SAM with initial cells in two zones is called duplex. The SAMs of some microphyllous lycopods, such as the Lycopodiaceae and Isoetaceae, have classification problems because there is no apparent apical cell but there are plural initials. These SAMs have been variously recognized as either monoplex (fern) (Newman, 1965
), Lycopodium type (Popham, 1951
), or seed-plant type (Philipson, 1990
). There is also controversy about whether the large superficial cell sometimes distinguished in the Isoetaceae SAM is an apical cell or not (Sam, 1984
, references cited therein). From the present examination, clearly Lycopodiaceae and Isoetaceae SAMs have IPD, supporting classification as Newman's (1965) simplex type or Philipson's (1990) seed-plant type. With respect to the PD network, SAMs of vascular plants can be classified into two groups: the fern-type SAM with a single apical cell, and the seed-plant-type SAM with plural apical initials.
The SAM of young Arabidopsis thaliana, which were cultivated in the phytotron, had the widest PD among plants examined. Perhaps PD diameter and PD density are affected by growth conditions or developmental stages. Whether the PD density changes under different growth conditions and/or through the ontogeny of the plant is still unclear, but that question is beyond the scope of the present examination.
PD network in relation to SAM evolution
Cooke et al. (1996)
stressed that the LPD and IPD are probably correlated with the absence or presence of the ability to form secondary PD, respectively. In LPD plants, PD densities in the cell walls of mature structures depend on the number of primary PD in the apical cell and the relative amount of wall expansion during cell growth. In contrast, most PD of IPD plants are probably of secondary origin, and their distribution depends more on specific intercellular interactions across shared walls, rather than on cell lineage and wall expansion. The primary and secondary PD may be morphologically indistinguishable (Ding et al., 1992
; Kragler et al., 1998
), because Y- and H-shaped PD, which are typical of secondary PD, can develop similarly in primary walls (Ehlers and Kollmann, 2001
). Although distinguishing secondary PD from primary PD is difficult, recent elegant examinations demonstrated actual formation of secondary PD for angiosperms (Bergmans et al., 1997
; Ormenese et al., 2000
) and the absence of secondary PD in the fern genus Azolla (Gunning, 1978
). If this strong correlation between IPD SAM and secondary PD is the case, lycopods with IPD SAMs (Lycopodiaceae and Isoetaceae) should have the ability to form secondary PD. We must clarify whether PD can develop secondarily in pre-existing walls in Lycopodiaceae and Isoetaceae.
Secondary PD seem to have a more complex development than primary PD (Kragler et al., 1998
, and references herein cited). They also probably differ from primary PD in their capacity to transfer specific macromolecular signals (Ding et al., 1992
; Perbal et al., 1996
; van der Schoot and Rinne, 1999b
). On the other hand, in fern SAMs with a single initial cell, the frequency of formation of primary PD appears to be precisely controlled during cytokinesis (Gunning, 1978
; Overall, 1999
). It seems likely that IPD and LPD networks are regulated by their own unique systems.
In the evolution of SAM structures, SAMs with a single apical cell are generally considered to be primitive and to have been the ancestral precursors of SAMs with plural initial cells (Popham, 1951
; Newman, 1965
; Mishler and Churchill, 1984
; Kato and Imaichi, 1997
). SAMs with plural initial cells probably have an advantage over SAMs with a single apical cell, because the increased number of initial cells can result in increased somatic mutation buffering when mutation rates are high (Klekowski, 1988
). Given this evolutionary scenario, Lycopodiaceae and Isoetaceae SAMs may have evolved the IPD network independently of seed plants (Fig. 6).
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argued that if secondary PD were lost, the need for all adjacent cells to communicate via their PD would provide a strong selection pressure for maintaining single apical cells in plants that have only primary PD.
Because there is almost no fossil evidence about the SAM structure of the early vascular plants and because the apex of Devonian Rhynia gwynne-vaughanii appears to be composed of closely packed cells with no single apical cell (Edwards, 1994
), there is a crucial need for data on PD networks of the apical meristem in the sporophytes of bryophyte sisters to vascular plants. There is one paper on the PD of Sphagnum leafy shoots (gametophytes), and it indicates a gradient in PD density (numbers per 1 µm not 1 µm2) from the apical cell to basal differentiated cells (Ligrone and Duckett, 1998
). Unlike the common apical cell in bryophyte gametophytes, bryophyte sporophytes may or may not have a single apical cell, depending on the class (Smith, 1955
; Schuster, 1984
; Crum, 2001
). Comparative analysis of bryophyte PD networks in a phylogenetic framework would be useful in understanding the evolutionary scenario of PD networks in land plants.
APPENDIX 1.
Species examined and their collection locality. All voucher specimens are housed in the Herbarium of the University of Tokyo, TI
FOOTNOTES
1 The authors thank N. Moritoki for technical assistance, M. Kato of the National Science Museum and anonymous reviewers for useful comments on the manuscript, and Y. Konno of Japan Women's University for help with statistical analyses. The authors are grateful to the staff of the University of Tokyo Botanical Gardens and Korakuen Garden for providing plant materials and to H. Tsukaya of the University of Tokyo and N. Nagata of Japan Women's University for providing Huperzia serrata and Arabidopsis seeds, respectively. This study was supported by Grants-in-Aid for Scientific Research (13640704) from the Japan Society for the Promotion of Science. 
4 Author for correspondence (e-mail: ryoko{at}fc.jwu.ac.jp
)
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