AOBPreview originally published online on May 30, 2006
Annals of Botany 2006 98(1):107-115; doi:10.1093/aob/mcl115
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The Unique Pollen Morphology of Duparquetia (Leguminosae: Caesalpinioideae): Developmental Evidence of Aperture Orientation Using Confocal Microscopy
1 Micromorphology Group, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE, UK and 2 Natural History Museum, Cromwell Road, London SW7 5BD, UK
* For correspondence. E-mail h.banks{at}rbgkew.org.uk
Received: 1 November 2005 Returned for revision: 14 February 2006 Accepted: 15 March 2006 Published electronically: 30 May 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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• Background and Aims The phylogenetic affinities of the aberrant monotypic genus Duparquetia (subfamily Caesalpinioideae) are at present unresolved. Preliminary results from molecular analyses suggest a basal, isolated position among legumes. A study of Duparquetia pollen was carried out to provide further morphological characters to contribute to multi-data set analyses. Understanding the development of Duparquetia pollen was necessary to clarify the orientation of the apertures.
• Methods Pollen grains and developing microspores were examined using light microscopy, confocal microscopy and scanning electron microscopy. Evidence for the orientation of the apertures was provided by the examination of microspores within developing tetrads, using (a) confocal microscopy to locate the position of the ectoapertures, and (b) light microscopy and Alcian blue stain to locate the position of the endoapertures.
• Key Results Confocal microscopy has been used for the first time to examine developing microspores in order to obtain information on ectoapertures that was unavailable using other techniques. Pollen in Duparquetia develops in tetrahedral tetrads as in other eudicots, with the apertures arranged in a modified pattern following Fischer's rule. Pollen grains are asymmetrical and have one equatorial-encircling ectoaperture with two equatorial endoapertures, a unique feature in Leguminosae, and in eudicots.
• Conclusions The pollen morphology of Duparquetia is so unusual that it provides little information to help determine its closest relatives. However, it does fit with a pattern of greater pollen morphological diversity in the first-branching caesalpinioid legume groups than in the more derived clades. The latitudinal ectoaperture of Duparquetia is unique within the Fabales and eudicot clades, resembling more closely the monosulcate pollen found in monocots and basal angiosperms; however, developmental patterns are recognizably similar to those of all other legume pollen types.
Key words: Duparquetia orchidacea, Leguminosae, pollen apertures, pollen development, confocal microscopy, tetrads
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INTRODUCTION |
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Work is in progress to assess and contribute pollen morphological data to a multidisciplinary phylogenetic study of the legume subfamily Caesalpinioideae (Banks and Klitgaard, 2000
; Banks et al., 2003). Duparquetia orchidacea Baill. has been targeted for multidisciplinary study, partly because the relationships of this isolated, monotypic, West African genus remain poorly understood, and partly because of its highly unusual floral morphology. Bentham (1865) described Oligostemon (a synonym of Duparquetia published in the same year that Baillon published Duparquetia) as ‘a perfectly isolated genus, combining characters from very different tribes’. Irwin and Barneby (1981) placed it in its own subtribe Duparquetiinae (tribe Cassieae). Duparquetia is a liana with imparipinnate leaves, a racemose inflorescence and zygomorphic flowers. It lacks vestured pits in the wood vessels, a feature that is present in most members of the Leguminosae except for the basal clade Cercideae and some members of the Dialiinae s.l. clade (Herendeen et al., 2003). Flowers of Duparquetia have four heteromorphic sepals and five heteromorphic petals. The vexillary petal is exterior in bud, which is a characteristic of subfamily Papilionoideae. A phylogenetic analysis based on morphological characters (Chappill, 1995) placed Duparquetia in a trichotomy with subfamily Papilionoideae. In the analyses of Herendeen et al. (2003), Duparquetia was resolved as sister to the Dialiinae s.l. clade with very weak (53 %) bootstrap support. Molecular and floral developmental data are being prepared for further phylogenetic analyses (Klitgaard et al., 2002; B. B. Klitgaard, unpubl. res.). Preliminary molecular phylogenies, incorporating trnL intron sequence data with the molecular analyses of Bruneau et al. (2001) based on rbcL sequences, confirm a basal position of Duparquetia in the Leguminosae (B. B. Klitgaard et al., unpubl. res.), although the closest relatives are at present uncertain.
Pollen morphology of Duparquetia was previously described and illustrated using scanning electron microscopy (SEM) by Graham et al. (1980) and Graham and Barker (1981). Ferguson (1987) illustrated the wall structure using transmission electron microscopy (TEM). However, the orientation of the grain (position of the distal and proximal poles) and therefore the relative position of the apertures was unknown, since developing tetrads had not been examined. Graham et al. (1980) and Graham and Barker (1981) regarded Duparquetia pollen as unlike anything in the Caesalpinioideae and possibly unique in the angiosperms (Fig. 1A–E, this study). Typical eudicot pollen is isopolar with compound, equatorial apertures based on the tri-aperturate pattern (Blackmore and Crane, 1988, 1998), and most eudicot pollen develops in tetrahedral tetrads following simultaneous cytokinesis, with the position of the apertures following Fischer's rule (Erdtman, 1969; Blackmore and Crane, 1988, 1998; Ressayre et al., 2002). Typical legume pollen also conforms to this pattern (Banks and Klitgaard, 2000). Duparquetia, on the other hand, has three prominent, meridionally elongated ridges that superficially resemble protruding apertures. There are two endoapertures assumed to be located one at each pole. The aim of the present investigation is to provide evidence of aperture orientation and symmetry so that the unusual pollen of Duparquetia can be compared with other legume pollen. This project is part of a larger multidisciplinary study that aims to add to the understanding of the evolution of the legumes and the complex systematics of the group (Banks and Klitgaard, 2000; Banks et al., 2003). Accurate assessment of homologous structures is required in order for pollen morphology to provide characters for phylogenetic analysis. Because the pollen morphology of Duparquetia is so different from that of other legume pollen, various new methods were needed to study developing microspores. Developmental studies were required in order to work out the orientation of the proximal and distal poles and thus the orientation of the apertures. The determination of polar or equatorial positioning of the ecto- and endoapertures is important so that a comparison of the pollen of Duparquetia can be made with other legume pollen. In order to do this, either previously used methods were adapted, such as the use of Alcian blue stain to study endoapertures (Banks, 2003), or new methods of study were developed. For the first time, confocal microscopy was employed to study developing microspores and locate the position and orientation of the ectoapertures.
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The confocal microscope has not been used to study pollen development before; however, it has been used in many biological and medical studies, in which a wide range of fluorescent dyes are applied to stain specific cell areas or cell organelles. Feist-Burkhardt and Pross (1998)
applied fluorescence confocal laser scanning microscopy for morphological analysis and imaging purposes to organic-walled microfossils from the Middle Jurassic (approx. 170 million years old). They successfully imaged unstained specimens as well as specimens stained with basic fuchsin, which is a common dye in palaeopalynology for increasing contrast in conventional transmitted light observation. Confocal microscopy has been shown to be a valuable tool in the morphological analysis of fossil palynomorphs such as pollen, spores and dinoflagellate cysts without special sample preparation (Feist-Burkhardt and Pross, 1998; Feist-Burkhardt and Monteil, 2001; Feist-Burkhardt et al., 2003; Hochuli and Feist-Burkhardt, 2004; Thouand et al., 2005). |
MATERIALS AND METHODS |
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Examination of the tetrad stage of Duparquetia pollen development
A collection of fresh material, comprising inflorescences with flower buds in all stages of development from one plant (Table 1), was fixed in glutaraldehyde and stored in 80 % ethanol. Anthers of various sizes were examined, and the ones that were approx. 7 mm long were found to contain microspores that were at the ideal stage for study. In these anthers, the microspores were in tetrads surrounded by callose envelopes. Larger anthers contained microspores with thin or missing callose so that the microspores were not held in tetrad formation when examined.
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A number of techniques were employed to study the developing microspores, in order to try and determine the position and orientation of the apertures. No single technique supplied a complete answer, and standard methods failed to provide any information at all; however, the following two newly devised methods were successful in providing data on the endoapertures and ectoapertures, respectively.
(1) Tetrads were removed from the anthers and stained with a 1 % solution of Alcian blue. A small cube of glycerol jelly mounted on a needle was used to pick up stained tetrads. The cube of jelly was mounted onto a light microscope (LM) slide and covered with a cover slip. The tetrads were then examined using LM.
(2) Duparquetia pollen tetrads were examined using the Leica TCS SP confocal microscope at the Natural History Museum, London. Both unstained tetrads and tetrads stained with basic fuchsin were mounted in glycerine between a slide and cover slip and analysed using a 40 x 1·0 NA oil PL Fluotar objective. Leica default ‘TRITC_wide’ filter settings of the confocal microscope were used to obtain fluorescence image stacks. This means that excitation takes place at a wavelength of 568 nm and emitted fluorescence light with a wavelength longer than 570 nm is detected. Images were captured with a lateral resolution of 1024 x 1024 pixels and a vertical distance between individual optical sections of 436 nm. The resulting image stacks were then processed using the Leica 3D rendering software to obtain extended focus images such as maximum projections, shadow projections, red/green anaglyphs and 3D animations. For further image processing and preparation of the photographic plates, NIH Image 1·61, ACD Canvas 9·0 and Adobe Photoshop 7·0 were used on an Apple PowerBook G4/1 GHz laptop computer with Mac OS x 10·2.8 and 1 Gbyte RAM.
Examination of mature Duparquetia pollen
Pollen from four collections from the herbarium of the Royal Botanic Gardens, Kew (Table 1) were examined using SEM, TEM and LM using standard preparation techniques (e.g. Banks and Gasson, 2000; Banks and Klitgaard, 2000).
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RESULTS |
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The tetrad stage of Duparquetia pollen development
Using LM alone, it was not possible to see the arrangement of the microspore ectoapertures due to the callose wall surrounding the tetrads. Various stains (saffranine, Alcian blue, malachite green, toluidine blue, Alexander's stain, Analine blue, Congo red and basic fuchsin) did not make the surface of the microspores within the tetrads or the aperture arrangement more visible. Acetolysis did remove the callose wall; however, the microspores were no longer held in tetrads, and so no information on orientation of the microspores could be obtained.
Observation of the microspores using Alcian blue stain for LM shows the orientation of the endoapertures within the tetrad (Fig. 3B–D).
Using confocal microscopy, all unstained tetrads and specimens stained with basic fuchsin yielded suitable images of the microspores in the tetrad. Material stained with other stains either did not provide enough fluorescence signal, or the callose envelope of the tetrad was too highly stained, obscuring the individual microspores within. In all specimens imaged with confocal microscopy, the organization of the microspores arranged in a tetrahedral tetrad is seen by focusing through the image stack (Fig. 2A–F). The three-dimensional arrangement is well illustrated in the extended focus image produced using SFP shadow projection (Fig. 2G), and less clearly visible in the extended focus images using maximum projection (Fig. 2H) or the red/green anaglyphs (Fig. 2I). This is mainly due to the small size of the tetrads with a thickness of only approx. 20 µm in the mounted slides. The tetrads may have suffered some minor compression during slide preparation. The cell contents of the microspores also showed a strong fluorescence, which impaired the detailed observation and analysis of the microspore wall and the orientation of the apertures. In the centre of each microspore, a circular zone with lower fluorescence intensity is visible which is the nucleus. The ectoapertures are equatorial and latitudinal in position (Fig. 2A–I, arrows).
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Duparquetia pollen develops in tetrahedral tetrads (Fig. 3B–D). Within the tetrad, the proximal pole of each microspore is narrower than the distal pole (Figs 2G–I and 3E). In most eudicots, the apertures occur in pairs at six points on the tetrad surface according to Fischer's rule (Erdtman, 1952
; Fig. 4A); endoapertures occur in pairs at four points in Duparquetia (Fig. 4B). To assist with the visualization of the layout of endoapertures, Erdtman diagrams (Erdtman, 1969) of Fisher's rule (Fig. 4D) and a comparative diagram of Duparquetia (Fig. 4E) are presented. These show the similarity between the layout of developing endoapertures of Duparquetia pollen to the Fischer's rule diagram; the endoapertures with matching positions are marked in red. The latitudinal positions of the equatorial ectoapertures are shown in Fig. 4C. The dissimilar proximal and distal poles of Duparquetia microspores and asymmetry (Figs 2 and 3) provide a rare opportunity to follow the development of microspores within the tetrad and determine aperture orientation.
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Description of mature Duparquetia pollen
Duparquetia pollen is small to medium in size (20–35 µm in diameter). There is one equatorial ectoaperture that completely encircles the grain, and two circular endoapertures each of approx. 1–2 µm in diameter (Fig. 1A–C, E). Three ridges are present. Two are parallel with and lying alongside the ectoaperture on the distal side of the grain; these protrude and make the grain longer in a lateral (equatorial) dimension. On the proximal side of the grain, one larger ridge lies halfway between the other two, and this protrudes in a vertical, polar dimension (Fig. 1A–C, E). Overall this gives the grain a triangular shape that can be observed during the tetrad stage (Fig. 2G–I). The ridges comprise dense and long columellae, a well-developed foot layer and thin endexine. The apertural zone comprises a thick endexine, no footlayer and a fine granular tectum (Fig. 1D). The endoapertures are located at the ends of the larger ridge, opposite each other across the shorter sides of the grain (Fig. 3E). The ornamentation is psilate to microrugulate–perforate with a granular apertural area. The apertural area is involved in harmomegathic reactions; when dehydrated, the ridges remain prominent but the apertural areas retract as the cell volume decreases (Fig. 3A).
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DISCUSSION |
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The developmental mechanisms controlling the ontogeny of Duparquetia pollen can be compared with those of the majority of other eudicots. The microspores develop in a tetrahedral arrangement (Fig. 3B), typical of other eudicots following simultaneous cytokinesis (Furness and Rudall, 2004
; Ressayre et al., 2005). A typical example of tetrad orientation in tricolporate legumes is illustrated by Bauhinia pollen (Fig. 1F); this is released in permanent tetrads (Ferguson and Banks, 1994). Tetrahedral tetrads can never be the result of successive cytokinesis (Penet et al., 2005), and so we presume, even though lack of suitable material prevents proof of the lack of a dyad stage, that simultaneous cytokinesis occurs in developing Duparquetia microspores. In the eudicot clade, successive cytokinesis has only been documented in the basal Proteales (Blackmore and Barnes, 1995) plus two anomalous genera, Rafflesia (Rafflesiaceae) and Griffithella (Podostemonaceae) (Furness and Rudall, 2004). Duparquetia is a liana that grows in Tropical West Africa; it is not grown in cultivation, and only a limited supply of specifically collected and fixed material was available for this study; obtaining more material for developmental studies is difficult.
The endoaperture arrangement in Duparquetia pollen tetrads is recognizable as a pattern that follows Fischer's rule (Fig. 4A–E). According to Fischer's rule, apertures form in an inter-radial position in pairs. This is the most widely documented aperture arrangement in the eudicots (Erdtman, 1969; Blackmore and Crane, 1988, 1998; Blackmore and Barnes, 1995; Ressayre et al., 2002, 2005; Furness and Rudall, 2004), although there are examples of minor variations (Blackmore and Crane, 1998), and one other aperture arrangement (Garside's rule) has been documented (Garside, 1946; Erdtman, 1969; Blackmore and Crane, 1988, 1998; Blackmore and Barnes, 1995; Ressayre et al., 2002; Furness and Rudall, 2004). According to Garside's rule, apertures are radial and formed in groups of three.
The number of apertures per pollen grain is a relatively plastic feature in the basal clades of caesalpinioid legumes when compared with that of the more derived clades (Banks et al., 2003). For example, in the most basal monophyletic clade Cercideae, the genus Bauhinia has species with pollen having from three to nine apertures (Ferguson and Pearce, 1986; Banks et al., 2003). Dajoz et al. (1991) suggested that the morphology of angiosperm pollen has evolved towards an increasing number of apertures, and showed that four-aperturate grains germinated faster than three-aperturate grains. An increase in aperture number offers a potential selective advantage because it increases the number of prospective germination sites, thus increasing the likelihood of contact between at least one germination site and the stigmatic surface. At the base of the eudicot clade, an apparently fundamental shift in aperture position from polar to equatorial apertures was coupled with an increase in aperture number. This transition could be one of the key innovations underlying eudicot success (Furness and Rudall, 2004). Although aperture number is positively correlated with pollen germination speed, it is negatively correlated with viability, and pollen with few apertures has a better survival rate (Till-Bottraud et al., 1999, 2001). Within subfamilies Caesalpinioideae and Papilionoideae, pollen with three apertures is the most widely represented, and presumably therefore the most successful. No other pollen found in the family Leguminosae or the Fabales clade has only two endoapertures. There are other examples in rosid dicots, although none are homologous with the endoaperture structure found in Duparquetia. For example, in Cuphea (Lythraceae), 23 of 250 species have diaperturate rather than triaperturate grains (Graham and Graham, 2000). The endoapertures develop at opposing poles of the grain where the three colpi converge; functional equatorial pores are not apparent. Morphologically based parsimony analyses indicate a single origin for all species with diaperturate pollen from trisyncolporate pollen (Graham and Graham, 2000). Other examples of diaperturate pollen are found in the genus Fuchsia (Onagraceae, the sister family to Lythraceae) (both Myrtales), where diaperturate pollen is the rule (Nowicke et al., 1984). In Proteaceae, three of 50 genera (Banksia and Dryandra and some species of Embothrium) have consistently diaperturate pollen (Erdtman, 1952). Dryandra pollen has successive cytokinesis with a distinct dyad stage followed by the formation of decussate or tetragonal tetrads (Blackmore and Barnes, 1995). In Moraceae, pollen is generally triaperturate, but a few genera of Ulmaceae and Urticaceae (including Ficus, Trema and Sarcopilea) have one or a few species characterized by diaperturate pollen (Erdtman, 1952).
The two endoapertures found in pollen of Duparquetia are orientated according to a slightly modified version of Fischer's rule (Fig. 4A–E). However, the presence of an equatorial latitudinal ectoaperture appears to be unique in the eudicots. It is interesting that the aperture morphology of Duparquetia pollen is consistent with an aberrant aperture pattern noted by Pozhidaev (1998, 2000). According to his hypothesis, it corresponds to the cell cytoplasm polarity just after cytokinesis, and could result from a mistiming of developmental processes, whereby the pollen wall develops relatively too early during ontogeny.
In the Fabales clade, which includes Leguminosae, Surianaceae, Quillajaceae and Polygalaceae (e.g. Savolainen et al., 2000), there are no other documented examples of a single equatorial ectoaperture, although some taxa in the Polygalaceae have one encircling endoaperture (Erdtman, 1952; Furness and Stafford, 1995, H. Banks, unpubl. res.), and there are odd legume taxa that have shorter ectoapertures, for example some porate species of Eperua, Arcoa (Banks and Klitgaard, 2000; Banks et al., 2003) and Browneopsis (Klitgaard and Ferguson, 1992). Kreunen and Osborne (1999) studied the development of pollen apertures in Nelumbo (an early-branching eudicot), where the majority of mature pollen grains are tricolpate; however, less common monosulcate and diaperturate grains are also reported. Co-occurring aperture types in Nelumbo have been suggested to be an important transition in angiosperm aperture number (Kuprianova, 1979). However, Kreunen and Osborne (1999) suggest that aperture variability in Nelumbo may be correlated with the lateness of aperture ontogeny in the genus, which they found to occur in the early free spore stage. The orientation of the non-tricolpate apertures of Nelumbo (polar or equatorial, longitudinal or latitudinal) is at present unknown. Tetragonal as well as tetrahedral tetrads were observed; therefore, it is also possible that the monosulcate and diaperturate grains could originate by successive cytokinesis. This is unlike Duparquetia pollen which develops in tetrahedral tetrads. The latitudinal orientation of the ectoaperture in Duparquetia is equivalent to a zonasulculus, an aperture type otherwise usually found in monocots and basal angiosperms below the eudicot node. Tricolpate pollen forms a synapomorphy for the eudicot clade. The eudicots are postulated to have evolved during the Cretaceous approx. 125 million years ago (Barremian–Aptian boundary, Lower Cretaceous) (Crane, 1985; Crane et al., 1986, 1995; Doyle and Hotton, 1991), prior to the major diversification and ecological radiation of angiosperms, with legumes being highly speciated by the Maastrichtian (70 million years ago) (Herendeen et al., 1992). The structure of Duparquetia pollen provides evidence that ectoaperture and endoaperture development are independent of each other. In the fossil record, sulci and then colpi appeared before compound apertures. Other examples to take into account towards this hypothesis include Moullava, one genus in the Caesalpinia group that has very similar pollen to the other genera in the group except for the reduction of the ectoapertures (Banks et al., 2003); pseudocolpi (absence of endoapertures) alternating with colpori in some species of Afzelia (Banks and Klitgaard, 2000); and both porate and colpate pollen in species of Bauhinia (Banks and Klitgaard, 2000; Banks et al., 2003).
A developmental model based on cytogenetic events that occur during meiosis (Ressayre et al., 2002, 2005) suggests that the combination of the timing of nuclear divisions relative to cytoplasmic divisions (cytokinesis can be successive, simultaneous or intermediate), orientation of the meiotic axes (forming tetragonal, rhomboidal, tetrahedral or decussate tetrads) and the way callose is deposited to form the cleavage walls during cytokinesis is sufficient to account for the most widespread patterns of aperture layout. Furthermore, Ressayre et al. (2005) show that cell plate formation progresses differently in monocots and eudicots. This is followed by callose deposition with each step being independent of the other, and that where cell plate formation and additional callose deposits do not progress in the same way; aperture sites coincide with the last points of callose deposition and not with the last points of contact between the cytoplasm of the dividing cells as previously suggested by Wodehouse (1935). Because the pollen of Duparquetia is similar to that of other legumes and the majority of eudicot pollen, with respect to simultaneous cytokinesis and forming tetrahedral tetrads, this model suggests that changes in the way additional callose is deposited following cytokinesis during the early tetrad stage are responsible for the differences in aperture layout seen in the mature pollen grains; therefore, extending our research into this area may be worthwhile. Due to the complexity of the ontogenetic system, the zonasulculus seen in Duparquetia pollen would logically be more likely to be convergent with basal angiosperm morphology than a reversion.
The asymmetrical pollen morphology of Duparquetia is unusual although not unique in the Fabales clade. The two genera Heterosamara (Paiva, 1998) in family Polygalaceae, and Labichea in tribe Cassieae of the legume subfamily Caesalpinioideae (Banks et al., 2003) also have asymmetrical pollen. There are no current models to explain how asymmetrical pollen might develop.
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CONCLUSIONS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSACKNOWLEDGEMENTSLITERATURE CITED |
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The pollen morphology of Duparquetia is so unusual that it does not assist the understanding of relationships with other legumes. It has in common with other legume pollen simultaneous cytokinesis, tetrahedral tetrads, the presence of both ecto- and endoapertures, and endoaperture development which follows Fischer's rule. However, no other legume pollen has only one ectoaperture, or only two endoapertures. The presence of the latitudinal ectoaperture in Duparquetia pollen is unique not only in Leguminosae, but also within Fabales, and probably within the eudicots, even though cytokinesis and the layout of the endoapertures are recognizably similar to other legume pollen types. The apomorphic pollen morphology of Duparquetia provides additional evidence for the general trends found by Banks et al. (2003)
, that the first branching caesalpinioid legume groups show greater pollen morphological diversity than the more derived clades. |
ACKNOWLEDGEMENTS |
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We thank William Hawthorne for collecting developing buds for this study, and Professor Steve Blackmore plus two other anonymous reviewers for their helpful comments.
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LITERATURE CITED |
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