Annals of Botany 92: 299-307, 2003
© 2003 Annals of Botany Company
The Placenta in Monoclea forsteri Hook. and Treubia lacunosa (Col.) Prosk: Insights into Placental Evolution in Liverworts
1 Dipartimento di Scienze ambientali, Seconda Università di Napoli, via A. Vivaldi 43, 81100 Caserta, Italyand 2 School of Biological Sciences, Queen Mary University of London, Mile End Road, London E1 4NS, UK
* For correspondence. E-mail roberto.ligrone{at}unina2.it
Received: 13 December 2002; Returned for revision: 31 March 2003; Accepted: 13 May 2003
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ABSTRACT |
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Placental morphology is remarkably diverse between major bryophyte groups, especially with regard to the presence and distribution of transfer cells in the sporophyte and gametophyte. In contrast, with the exception of metzgerialean liverworts, placental morphology is highly conserved within major bryophyte groups. Here we examine the ultrastructure of the placenta in Monoclea forsteri and Treubia lacunosa, basal members of the marchantialean and metzgerialean liverwort lineages, respectively. In both species several layers of transfer cells are found on both sides of the placenta, with sporophytic transfer cells exhibiting prominent wall labyrinths. Consistent with previous reports of a similar placenta in other putatively basal and isolated liverwort genera such as Fossombronia, Haplomitrium, Blasia and Sphaerocarpos, this finding suggests that this type of placenta represents the plesiomorphic (primitive) condition in liverworts. Distinctive ultrastructural features of placental cells in Monoclea include branched plasmodesmata in the sporophyte and prominent arrays of smooth endoplasmic reticulum, seemingly active in secretion in the gametophyte. These arrays contain a core of narrow tubules interconnected by electron-opaque rods, structures with no precedent in plants. Analysis of the distribution of different types of placenta in major bryophyte groups provides valuable insights into their inter-relationships and possible phylogeny.
Key words: Bryophyte phylogeny, endoplasmic reticulum, liverworts, Monoclea, placenta, transfer cells, Treubia.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Nutritional dependence of the sporophyte on the gametophyte (matrotrophy) is a distinctive feature of the embryophytes (syn. land plants). Nutrients are actively transferred to the sporophyte across a specialized area that develops at the junction between the two generations, the placenta (Graham and Wilcox, 2000).
In contrast to the tracheophytes, the sporophyte in bryophytes is permanently associated with the gametophyte and retains structural, if not functional, dependence throughout its life span. The placenta in bryophytes is a particularly prominent and highly differentiated structure.
Ultrastructural research (reviewed in Ligrone et al., 1993; Frey et al., 2001) has revealed that the placental organization is remarkably diverse between major bryophyte groups but that, with the exception of simple thalloid liverworts (i.e. the order Metzgeriales according to Bartholomew-Began, 1990), it shows only minor intra-group variation. The most important diagnostic feature is the distribution of transfer cells. These are found on both sides of the placenta in the bryalean mosses and marchantialean liverworts as well as in Haplomitrium, but only on the sporophytic side in the Takakiales, Andreaeales and Polytrichales among the mosses. In the leafy liverworts (Jungermanniidae), they are only on the gametophytic side in the anthocerotes, and are absent on both sides in the Sphagnales (Ligrone et al., 1993). In contrast, all possible types of transfer cell distribution have been found in the metzgerialean liverworts investigated to date. Transfer cells occur on both sides of the placenta in Fossombronia and Blasia (Ligrone et al., 1993), only in the sporophyte in Pallavicinia (Ligrone et al., 1993), Symphyogyna (Frey et al., 1996) and Apotreubia (Frey and Hilger, 2001), only in the gametophyte in Riccardia (Ligrone et al.,1993), and are absent from both generations in Pellia, Aneura, Cryptothallus (Ligrone et al., 1993), Hymenophyton (Frey et al., 1996) and Metzgeria (Frey et al., 2001).
Molecular and morphological evidence supports the liverworts as a monophyletic group, although their relationships with the other embryophytes are still debated (Garbary and Renzaglia, 1998; Hedderson et al., 1998; Nickrent et al., 2000). This implies that the different types of placenta in liverworts have a common origin from a plesiomorphic (primitive) condition.
With the aim of gaining insights about this condition, we investigated the placenta in two species collected during a recent expedition to New Zealand, Treubia lacunosa (Col.) Prosk and Monoclea forsteri Hook., both representatives of ancient liverwort lineages (Schuster, 1984).
Treubia, along with the allied genus Apotreubia, is currently classified in the subclass Metzgeriidae, along with simple thalloid liverworts (Crandall-Stotler and Stotler, 2000) but presents affinities with both jungermannialean (the leafy habit) and marchantialean liverworts (oil bodies confined to specialized idioblasts) (Schuster and Scott, 1969; Schuster, 1984). Blepharoplast morphology supports an isolated position of this group and also emphasizes important affinities with Haplomitrium (Carothers and Rushing, 1990). Molecular analysis, based on a plastid DNA intron, has shown that Treubia and Apotreubia do not cluster with the jungermanniopsid or the marchantiopsid line but form a distinct clade referred to as the Treubiopsida (Stech et al., 2000; Stech and Frey, 2001).
The genus Monoclea includes only two species, M. forsteri, restricted to New Zealand, and M. gottschei Lindb. occurring in Central and South America (Gradstein et al., 1992; Meißner et al., 1998). Together these form the monogeneric order Monocleales currently classified in the Marchantiidae (Crandall-Stotler and Stotler, 2000), a position also confirmed by molecular analysis (Stech et al., 2000; Wheeler, 2000); however, Monoclea also presents affinities with the Metzgeriidae, notably the simple morphology of the thallus (i.e. the absence of air chambers, specialized archegoniophores and pegged rhizoids) and the extensive elongation of the seta following capsule maturation (Campbell, 1954, 1984; Schuster, 1984; Duckett et al., 2000).
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MATERIALS AND METHODS |
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Plants of Treubia lacunosa and Monoclea forsteri, bearing young and maturing sporophytes, were collected in September 2001 from earth banks in mixed podocarp forests near Ross (170°48'E, 42°54'S) and Harihari (170°34'E, 43°09'S), Westland, South Island, New Zealand.
The samples were immediately transferred to the laboratory and processed for electron microscopy. Only the youngest sporophytes with unelongated setae were used. At this stage the capsules contained either dividing sporocytes or just formed tetrads in both species. The placental region, including the sporophyte foot and surrounding gametophyte tissue, was cut longitudinally into thin slices under a dissecting microscope in a drop of fixative (2 % glutaraldehyde, 1 % freshly-prepared formaldehyde and 0·75 % tannic acid in 0·04 M piperazine-N,N'–bis(2-ethanesulfonic acid) (PIPES) buffer, pH 7·0, and transferred to a larger volume of the same fixative in scintillation vials for 2 h at room temperature under gentle vacuum. The samples were then rinsed in 0·08 M PIPES buffer and twice in 0·08 M Na-cacodylate buffer and post-fixed in 1 % OsO4 in 0·08 M Na-cacodylate buffer, pH 6·7, overnight at 4 °C. Following dehydration in a step gradient of ethanol with three exchanges of anhydrous ethanol and one of propylene oxide at 4 °C, the samples were slowly infiltrated with Spurr’s resin at 4 °C, transferred to polypropylene dishes and cured at 68 °C for 24 h. Thin sections were cut with a diamond knife, stained with 3 % uranyl acetate in 50 % methanol for 15 min and in Reynold’s lead citrate for 10 min, and observed with a Philips E-208 electron microscope. For light microscopy, 0·5-µm-thick sections were cut with a diamond histoknife, stained with 0·5 % toluidine blue and photographed with a Zeiss Axioskop light microscope equipped with a Sensicam photocamera.
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RESULTS |
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In both Monoclea and Treubia the sporophyte arises subapically and has a massive seta with a relatively small foot of bulbous shape (Fig. 1A and B). The transition between the foot and seta in Monoclea is slightly narrowed, suggesting the presence of a rudimentary collar (Fig. 1A). In both species there are several layers of cells with labyrinthine walls (transfer cells) on both the sporophytic and gametophytic side of the placenta (Fig. 1C and D). In Monoclea, healthy transfer cells of sporophytic and gametophytic origin are close to each other (Figs 1C and 2A). In Treubia the two generations are separated by a wide space, including several layers of dead collapsed cells of gametophytic origin (Figs 1D and 2B).
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In Monoclea the foot epidermal cells have highly branched and coarse wall ingrowths that form a wall labyrinth, closely similar in complexity and morphology to the extensive wall labyrinth typical of the sporophyte in marchantialean liverworts (Fig. 2A). The wall ingrowths in sporophytic transfer cells in Treubia are relatively thin and the extension of the wall labyrinth varies from cell to cell (Fig. 2B). The cytoplasm associated with wall ingrowths in Treubia contains elements of rough endoplasmic reticulum (ER) (Fig. 3A). In both species the gametophytic cells of the placenta generally have less prominent wall labyrinths than sporophytic cells.
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As is typical of placental cells in most bryophytes, the plastids are scarcely differentiated and lack (Fig. 3B) or contain only a rudimentary inner membrane system (Fig. 3C). The plastids in gametophyte placental cells in Treubia are always segregated in cytoplasmic areas far from the wall labyrinth (not shown). The mitochondria in sporophytic placental cells are distinctly larger and have less electron-opaque stroma than their gametophytic counterparts, especially in Treubia (Fig. 3C and D).
A high concentration of plasmodesmata is visible in the inner tangential walls of sporophytic transfer cells as well as in the walls of more internal cells of the foot. The plasmodesmata in Monoclea are often branched (Fig. 3E) and swollen in their middle part. Adjacent swollen plasmodesmata or plasmodesmal branches may either merge together, thus producing prominent cavities in the inside of the walls (Fig. 3F), or remain close to each other to form distinctive honeycomb profiles (Fig. 3G).
A highly distinctive feature of gametophytic transfer cells in Monoclea is the presence of conspicuous arrays of tubular smooth ER (Figs 2A and 4A). These arrays contain a core of narrower membranous tubules linked to each other by electron-opaque rods about 10 nm thick and 60 nm long (Fig. 4B and C). The cytoplasm contains a great number of vesicles ranging from less than one to several micrometres in diameter. The bigger vesicles, of irregular shape, are often seen to merge with the plasmalemma outlining the wall ingrowths (Fig. 4A). The cells contain relatively few dictyosomes and abundant coated vesicles associated with partially coated reticulum (Fig. 4D).
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DISCUSSION |
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The discovery of a typical marchantialean placenta in M. forsteri confirms former observations on M. gottschei (Ligrone et al., 1993) and is coherent with current classification of the Monocleales in the Marchantiidae. A marchantialean placenta also occurs in Blasia among the metzgerialean liverworts (Ligrone et al., 1993). On the other hand, the placental morphology in Treubia, characterized by the presence of transfer cells with thin wall ingrowths in both generations and several layers of collapsed gametophyte cells, is strongly reminiscent of the placenta in Fossombronia and Haplomitrium (Ligrone et al., 1993). Our observations on Treubia lacunosa contrast with the report of transfer cells being restricted to the sporophyte in the allied species Apotreubia hortonae (Frey and Hilger, 2001). In line with molecular evidence (Stech et al., 2002), this is an indication of wide divergence between the two genera.
Along with Haplomitrium, Fossombronia, Blasia and Sphaerocarpos, Monoclea and Treubia represent ancient lineages considered to be remnants of the early diversification of the liverwort clade (Schuster, 1984; Crandall-Stotler and Stotler, 2000; Stech and Frey, 2001). It is noteworthy that three of them, Haplomitrium, Monoclea and Blasia, share monoplastidic meiosis, a character considered to be a symplesiomorphy (shared primitive feature) of embryophytes and coleochaetalean algae (Renzaglia et al., 1994). In a cladistic analysis based on male gametogenesis, Treubia forms a clade with Haplomitrium (Garbary et al., 1993), whilst a study based on a large number of morphological and biochemical characters supports a clade of Haplomitrium with Monoclea (Garbary and Renzaglia, 1998), both results being at odds with conclusions from molecular studies (Stech et al., 2000; Wheeler, 2000; Stech and Frey, 2001). In a cladistic analysis based uniquely on morphological characters (Crandall-Stotler and Stotler, 2000), Monoclea was assigned a basal position within the marchantialean liverworts, but it was considered an advanced taxon on the basis of molecular data (Wheeler, 2000). The results of molecular analysis demand re-evaluation of the apparent morphological simplicity of Monoclea (notably the absence of air spaces and pegged rhizoids, the latter feature also shared with aquatic Riccia spp. and Neohodgsonia), in terms of adaptation to extremely moist and stable habitats (Bischler-Causse et al., 1995; Duckett et al., 2000). Other features of Monoclea, viz. the absence of specialized archegoniophores, the extensive elongation of the sporophyte seta emerging from the main thallus and monoplastidic meiosis, are almost certainly primitive.
The fact that all the six taxa considered above, otherwise widely divergent for a number of morphological, developmental and molecular characters, share the same basic type of placenta with transfer cells in both generations, strongly suggests that this condition has been inherited from a common ancestor and is a plesiomorphy in liverworts. It is suggested that, with the only known exception of Riccia, a highly derived genus (Wheeler, 2000), this type of placenta has been retained in the whole marchantioid lineage (Ligrone et al., 1993). In contrast, it is suggested that all other types of placenta in liverworts have arisen by reduction, i.e. disappearance of transfer cells from one or both generations. The extreme variability of placental morphology in simple thalloid liverworts mirrors a similar diversity in sperm morphology (Renzaglia and Duckett, 1991) and might suggest polyphyly, were it not for the fact that here even closely allied genera such as Riccardia and Aneura may exhibit different placental morphologies.
The available evidence indicates that a different type of placenta, with transfer cells in the sporophyte only, is the plesiomorphic condition in mosses (Ligrone et al., 1993). The conclusion that liverworts and mosses do not share a plesiomorphic type of placenta is compatible with phyletic trees where these are resolved as sister groups (see, for example, Garbary and Renzaglia, 1998; Hedderson et al., 1998; Goffinet, 2000; Nickrent et al., 2000; Renzaglia et al., 2000), but it implies that separation from a common ancestor must have involved a change in placental structure in either the liverwort or, perhaps more likely, the moss lineage. In contrast, the highly distinctive type of placenta present in the anthocerotes (viz. haustorial sporophytic cells and wall ingrowths restricted to the gametophyte) strongly supports separation of this group from both liverworts and mosses (Ligrone et al., 1993).
Figure 5 illustrates the distribution and possible interrelationships of four basic types of placenta in the major bryophyte groups. The type-1 placenta, found in a member of the putative green algal ancestor of the embryophytes, Coleochaete (Graham and Wilcox, 1983; Graham and Kaneko, 1991) and in the anthocerotes, is suggested to be the plesiomorphic condition in embryophytes. Based on this assumption, the anthocerotes are placed in a basal position, a situation consistent with other recent analyses based on morphological, biochemical and molecular data, not including placental morphology (Garbary and Renzaglia, 1998; Hedderson et al., 1998; Goffinet, 2000; Renzaglia et al., 2000). In contrast, our interpretation of the placental data, following Occam’s razor, does not fit well with other trees showing liverworts as the basal lineage of land plants (Kenrick and Crane, 1997; Nickrent et al., 2000; for a review of earlier work, see also Goffinet, 2000). The type-2 placenta, widespread in extant lower tracheophytes (cf. Frey et al., 2001; Duckett and Ligrone, 2003) and liverworts, is suggested to be an apomorphy (derived feature) of the liverwort/moss-polysporangiophyte clade (cf. Goffinet, 2000). Starting from this condition, a type-3 placenta arose independently in the moss and leafy liverwort lineages. Types 1, 3 and 4, which occur in the Metz geriidae, are also considered to be derived, directly or indirectly, from type 2. Within the moss lineage, type 2, present in the Bryopsida and Tetraphidales, has probably arisen secondarily from the type-3 condition. The clustering of the Tetraphidales (viz. Tetraphis, Buxbaumia and Diphyscium) with the Bryopsida, instead of the Polytrichales (cf. Hedderson et al., 1998), is consistent with a recent detailed analysis of moss phylogeny (Newton et al., 2000). The type-4 placenta in the Sphagnopsida is also considered a derived condition. However, the hypobasal origin of the foot in this group (Roth, 1969), contrasting with the epibasal origin in the other mosses, calls into question the homology of the sphagnalean placenta with other types of placenta (Ligrone et al., 1993). A hypobasal origin is also assumed by some authors (for example, Schuster, 1984) for the sporophyte foot and seta in the Sphaerocarpales and Marchantiales. Because of the paucity of developmental information available, this assumption is entirely subjective, and a simple alternative interpretation of the distinctive embryogeny in the Sphaerocarpales and Marchantiales favours a unitary basic pattern of early embryogeny in the liverwort/moss clade (Ligrone et al., 1993).
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Whether functional differences result from the morphological variability of the placenta in bryophytes is not known. The presence of a wall labyrinth is thought to enhance nutrient translocation by plasmalemma-associated carriers by both amplifying the overall surface area of the plasmalemma and maintaining a steeper concentration gradient in the apoplast between source and sink (Gunning and Pate, 1974; Ligrone and Gambardella, 1988). A placenta with transfer cells in both generations occurs both in taxa with an elongated seta, such as Haplomitrium, Blasia and Monoclea, and in those with a short seta and sporophytes on archegoniophores, i.e. most marchantialean liverworts. Reduction of the sporophyte apparently involved the disappearance of a foot and placental transfer cells in Riccia (Ligrone et al., 1993). On the other hand, transfer cells are also lacking in certain metzgerialean liverworts (e.g. Pellia and Cryptothallus) with exceedingly large sporophytes (Ligrone et al., 1993). We can conclude that the lack of transfer cells from one or both sides of the placenta does not necessarily imply a lower efficiency in terms of nutrient translocation; rather this suggests that hitherto unrecognized adjustments in the mechanism of nutrient translocation might have compensated for, or even triggered, the disappearance of transfer cells in certain lineages. Further analysis based on comparative data on fern placenta is presented in Duckett and Ligrone (2003).
It is pertinent to note that the development of a wall labyrinth in cultured cells of maize was found to involve no major change in wall composition (DeWitt et al., 1999), suggesting that the shift from non-labyrinthine to labyrinthine walls, or vice versa, depends more closely on adjustments in morphogenetic mechanisms than in biosynthetic pathways. Our current work, using monoclonal antibodies against cell wall components, may produce new information on the biochemistry of wall ingrowths that may further clarify homologies, as recently demonstrated for water-conducting cells (Ligrone et al., 2002). Because of the variability in closely related taxa, in-depth examination of simple thalloid liverworts has the greatest potential to shed light on the evolution of placental structure and function.
The presence of labyrinthine walls in collapsed gametophyte cells in Treubia indicates that these are placental transfer cells crushed down by the expanding foot. Collapsed gametophyte cells occurring in the placental space is a typical feature of the placenta in bryophytes, although not present in certain taxa, including Monoclea, and it was suggested to be a major character distinguishing the bryophyte lineage from tracheophytes (Frey et al., 2001). However, the recent report of collapsed gametophyte cells in the placenta of Isoëtes (Hilger and Frey, 2002) challenges this hypothesis.
In addition to Treubia, sporophytic mitochondria larger than their gametophytic counterpart have been reported in Calobryum blumei Nees [syn. Haplomitrium blumii (Nees) Schuster] (Ligrone et al., 1993). Re-examination of published and unpublished micrographs suggests that mitochondrial dimorphism may be a general feature of bryophyte life cycles.
The report of branched plasmodesmata in Monoclea is the first one for bryophytes, though specialized plasmodesmata have been described in food-conducting cells in both mosses and liverworts (Ligrone et al., 2000). Branched plasmodesmata are common in higher plants, notably in vascular tissues (Lucas et al., 1993; Glockmann and Kollmann, 1996).
The extensive system of smooth ER in gametophyte transfer cells in Monoclea has no precedent in placental cells of other bryophytes and is indicative of ER-mediated secretory activity. Extracellular secretion involving ER in cells with wall ingrowths has been reported in some higher plants, although it does not seem to be common (Kronestedt-Robards and Robards, 1991). Nutrient translocation from the gametophyte to the sporophyte in bryophytes is known to involve active transport of simple molecules and ions through the wall/membrane apparatus of placental cells (Renault et al., 1990, 1992). The ultrastructural evidence presented in this report suggests that gametophyte/sporophyte nutrient relationships in Monoclea may also involve secretion by exocytosis. Although at least 16 different ER domains have been described in plant cells (Staehelin, 1997), and several variants have been reported in specific tissues, notably sieve elements (Evert and Russin, 1991; Behnke, 1996), we are aware of no previous report of an ER array comparable with the cross-bridged tubular aggregations found in gametophyte placental cells of Monoclea. Intercisternal proteinaceous bridges are a normal feature of the Golgi system both in plant and animal cells and have been shown to be responsible for the stability of dictyosomal stacks (Cluett and Brown, 1992). A similar function, that is ensuring the stability of a specialized ER domain, is possible for the ER-associated bridges in Monoclea.
This study confirms placental morphology as a valuable character for defining the phylogeny and interrelationships of bryophytes and lower tracheophytes.
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ACKNOWLEDGEMENTS |
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Ultrastructural observations were carried out at the CISME (University of Naples ‘Federico II’, Italy). Thanks are extended to the Department of Plant and Microbial Sciences, University of Canterbury, Christchurch (New Zealand), for providing laboratory facilities and to the New Zealand Department of Conservation for granting collecting permits in National Parks. R.L. acknowledges a grant from CNR (Italy) supporting a short-term stay in New Zealand (in 2001).
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