Diversity and evolution of floral structure among early diverging lineages in the Ericales

This is a combination of review and original data on floral structure and diversity in the two earliest diverging lineages of the Ericales, i.e. the balsaminoids, comprising Balsaminaceae, Marcgraviaceae and Tetrameristaceae, and the polemonioids, comprising Fouquieriaceae and Polemoniaceae. Each clade is strongly supported in molecular studies, while structural synapomorphies have largely been lacking. For the balsaminoid families, we compare floral morphology, anatomy and histology among selected taxa and find that the entire clade is strongly supported by the shared presence of nectariferous tissue in the floral periphery, thread-like structures on anthers, truncate stigmas, secretion in the ovary, as well as mucilage cells, raphides and tannins in floral tissues. A possible sister group relationship between Balsaminaceae and Tetrameristaceae is supported by the shared presence of post-genital fusion of filaments and ovary and a star-shaped stylar canal. For polemonioids, we document unexpected diversity of floral features in Polemoniaceae, partly providing structural links to Fouquieriaceae. Features include cochlear and quincuncial corolla aestivation, connective protrusions, ventrifixed anthers and nectariferous tissue in the base of the ovary. In addition, we outline future directions for research on floral structure in the Ericales and briefly discuss the general importance of structural studies for our understanding of plant phylogeny and evolution.     

Palynological variation in Balsaminoid Ericales. II. Balsaminaceae, Tetrameristaceae, Pellicieraceae and general conclusions

BACKGROUND AND AIMS: The objective of this study is to examine the palynological diversity of Balsaminaceae (two genera/+/-1000 species), Tetrameristaceae (two genera/two species) and Pellicieraceae (one genus/one species). The diversity found will be used to infer the systematic value of pollen features within the balsaminoid clade. METHODS: Pollen morphology and ultrastructure of 29 species, representing all families of the balsaminoid clade except Marcgraviaceae, are investigated by means of light microscopy, scanning electron microscopy and transmission electron microscopy. KEY RESULTS: Balsaminaceae pollen is small to medium sized with three to four apertures, which can be either colpate or porate, and a sexine sculpturing varying from coarsely reticulate to almost microreticulate. Tetrameristaceae pollen is small sized, 3-colporate, with a heterobrochate reticulate sculpturing and granules present in the lumina. Pellicieraceae pollen is large sized, 3-colporate with long ectocolpi and a perforate sexine sculpturing with large verrucae. Furthermore, Pelliciera is characterized by the occurrence of aggregated orbicules, while orbicules are completely absent in both Balsaminaceae and Tetrameristaceae. Balsaminaceae pollen differs from the other balsaminoid families due to the occurrence of colpate or porate grains with an oblate to peroblate shape, a very thin foot layer and a lamellated endexine. CONCLUSIONS: From a pollen morphological point of view, Balsaminaceae are completely different from the other balsaminoid families. Therefore, no pollen morphological synapomorphies could be defined for the balsaminoid clade. However, various pollen features were observed that could indicate a possible relationship between Tetrameristaceae, Pellicieraceae and Marcgraviaceae. Despite the palynological similarities in the latter three families, it remains unclear to what extent they are related to each other.     

Conflicting phylogenies of balsaminoid families and the polytomy in Ericales: combining data in a Bayesian framework

The balsaminoid Ericales, namely Balsaminaceae, Marcgraviaceae, Tetrameristaceae, and Pellicieraceae have been confidently placed at the base of Ericales, but the relations among these families have been resolved differently in recent analyses. Sister to this basal group is a large polytomy comprising all other families of Ericales, which is associated with short internodes. Because there are more than 13 kb of sequences for a large sampling of representatives, a thorough examination of the available data with novel methods seemed in place. Because of its computational speed, Bayesian phylogenetics allows for the use of parameter-rich models that can accommodate differences in the evolutionary process between partitions in a simultaneous analysis. In addition, there are recently proposed Bayesian strategies of assessing incongruence between partitions. We have applied these methods to the current problems in Ericales phylogeny, taking into account reported pitfalls in Bayesian analysis such as model selection uncertainty. Based on our results we infer several, previously unresolved relationships in the order Ericales. In balsaminoid families, we find that the closest relatives of Balsaminaceae are Marcgraviaceae. In the Ericales polytomy, we find strong support for Pentaphylacaceae sensu APG II as the sister group of Maesaceae. In addition, Symplocaceae receive a position as sister to Theaceae and these families form a monophyletic group together with Styracaceae-Diapensiaceae. At the base of this clade are Actinidiaceae and Clethraceae. The positions of Ebenaceae and Lecythidaceae remain uncertain.     

The multiple fuzzy origins of woodiness within Balsaminaceae using an integrated approach. Where do we draw the line?

Background and Aims

The family Balsaminaceae is essentially herbaceous, except for some woodier species that can be described as ‘woody’ herbs or small shrubs. The family is nested within the so-called balsaminoid clade of Ericales, including the exclusively woody families Tetrameristaceae and Marcgraviaceae, which is sister to the remaining families of the predominantly woody order. A molecular phylogeny of Balsaminaceae is compared with wood anatomical observations to find out whether the woodier species are derived from herbaceous taxa (i.e. secondary woodiness), or whether woodiness in the family represents the ancestral state for the order (i.e. primary woodiness).

Methods

Wood anatomical observations of 68 Impatiens species and Hydrocera triflora, of which 47 are included in a multigene phylogeny, are carried out using light and scanning electron microscopy and compared with the molecular phylogenetic insights.

Key Results

There is much continuous variation in wood development between the Impatiens species studied, making the distinction between herbaceousness and woodiness difficult. However, the most woody species, unambiguously considered as truly woody shrubs, all display paedomorphic wood features pointing to secondary woodiness. This hypothesis is further supported by the molecular phylogeny, demonstrating that these most woody species are derived from herbaceous (or less woody) species in at least five independent clades. Wood formation in H. triflora is mostly confined to the ribs of the stems and shows paedomorphic wood features as well, suggesting that the common ancestor of Balsaminaceae was probably herbaceous.

Conclusions

The terms ‘herbaceousness’ and ‘woodiness’ are notoriously difficult to use in Balsaminaceae. However, anatomical observations and molecular sequence data show that the woodier species are derived from less woody or clearly herbaceous species, demonstrating that secondary woodiness has evolved in parallel.     

Relationships within balsaminoid Ericales: a wood anatomical approach

Wood samples of 49 specimens representing 31 species and 11 genera of woody balsaminoids, i.e., Balsaminaceae, Marcgraviaceae, Pellicieraceae, and Tetrameristaceae, were investigated using light microscopy and scanning electron microscopy. The wood structure of Marcgraviaceae, Pellicieraceae, and Tetrameristaceae is characterized by radial vessel multiples with simple perforation plates, alternate vessel pitting, apotracheal and paratracheal parenchyma, septate libriform fibers, and the presence of raphides in ray cells. Tetrameristaceae and Pellicieraceae are found to be closely related based on the occurrence of unilaterally compound vessel-ray pitting and multiseriate rays with long uniseriate ends. The narrow rays in Pelliciera are characteristic of this genus, but a broader concept of Tetrameristaceae including Pelliciera is favored. Within Marcgraviaceae, wide rays (more than five-seriate) are typical of the genus Marcgravia. Furthermore, there is evidence that the impact of altitude and habit plays an important role in the wood structure of this family. The wood structure of Balsaminaceae cannot be compared systematically with other balsaminoids because of their secondary woodiness. Balsaminaceae wood strongly differs due to the presence of exclusively upright ray cells in Impatiens niamniamensis, the absence of rays in Impatiens arguta, and the occurrence of several additional paedomorphic features in both species.     

Phylogenetic relationships in the order Ericales s.l.: analyses of molecular data from five genes from the plastid and mitochondrial genomes

Phylogenetic interrelationships in the enlarged order Ericales were investigated by jackknife analysis of a combination of DNA sequences from the plastid genes rbcL, ndhF, atpB, and the mitochondrial genes atp1 and matR. Several well-supported groups were identified, but neither a combination of all gene sequences nor any one alone fully resolved the relationships between all major clades in Ericales. All investigated families except Theaceae were found to be monophyletic. Four families, Marcgraviaceae, Balsaminaceae, Pellicieraceae, and Tetrameristaceae form a monophyletic group that is the sister of the remaining families. On the next higher level, Fouquieriaceae and Polemoniaceae form a clade that is sister to the majority of families that form a group with eight supported clades between which the interrelationships are unresolved: Theaceae-Ternstroemioideae with Ficalhoa, Sladenia, and Pentaphylacaceae; Theaceae-Theoideae; Ebenaceae and Lissocarpaceae; Symplocaceae; Maesaceae, Theophrastaceae, Primulaceae, and Myrsinaceae; Styracaceae and Diapensiaceae; Lecythidaceae and Sapotaceae; Actinidiaceae, Roridulaceae, Sarraceniaceae, Clethraceae, Cyrillaceae, and Ericaceae.     

Comparative floral structure and systematics in Crossosomatales (Crossosomataceae, Stachyuraceae, Staphyleaceae, Aphloiaceae, Geissolomataceae, Ixerbaceae, Strasburgeriaceae)

Floral structure of all putative families of Crossosomatales as suggested by molecular studies was comparatively studied. The seven comprise Crossosomataceae, Stachyuraceae, Staphyleaceae, Aphloiaceae, Geissolomataceae, Ixerbaceae, and Strasburgeriaceae. The entire clade (1) is highly supported by floral structure, also the clades (in sequence of diminishing structural support): Ixerbaceae/Strasburgeriaceae (2), Geissolomataceae/Ixerbaceae/Strasburgeriaceae (3), Aphloiaceae/Geissolomataceae/Ixerbaceae/Strasburgeriaceae (4), and Crossosomataceae/Stachyuraceae/Staphyleaceae (5). Among the prominent floral features of Crossosomatales (1) are solitary flowers, presence of a floral cup, imbricate sepals with outermost smaller than inner, pollen grains with horizontally extended endoapertures, shortly stalked gynoecium, postgenitally united carpel tips forming a compitum, stigmatic papillae two‐ or more‐cellular, ovary locules tapering upwards, long integuments forming zigzag micropyles, cell clusters with bundles of long yellow crystals, mucilage cells, seeds with smooth, sclerified testa and without a differentiated tegmen. Clade (2) is characterized by large flowers, petals forming a tight, pointed cone in bud, stamens with long, stout filaments and sagittate anthers, streamlined, conical gynoecium, antitropous ovules, rudimentary aril, lignified, unicellular, T‐shaped hairs and idioblasts with striate mucilaginous cell walls. Clade (3) is characterized by alternisepalous carpels, punctiform stigma formed by postgenitally united and twisted carpel tips, synascidiate ovary, only one or two pendant ovules per carpel, nectary recesses between androecium and gynoecium. Clade (4) is characterized by pronounced ‘pollen buds’. Clade (5) is characterized by polygamous or functionally unisexual flowers, x‐shaped anthers, free and follicular carpels (not in Stachyuraceae). Crossosomataceae and Aphloiaceae, although not retrieved as a clade in molecular studies, share several special floral features: polystemonous androecium; basifixed anthers without a connective protrusion; stigma with two more or less decurrent crests; camplyotropous ovules and reniform seeds; simple, disc‐shaped nectaries and absence of hairs. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 147 , 1–46.     

Morphology of Maundia supports its isolated phylogenetic position in the early‐divergent monocot order Alismatales

According to recent molecular phylogenetic data, the rare Australian endemic Maundia triglochinoides does not form a clade with taxa traditionally classified as members of Juncaginaceae. Therefore, views on the morphological evolution and taxonomy of Alismatales require re‐assessment. As the morphology of Maundia is poorly known and some key features have been controversially described in the literature, the flowers, fruits, inflorescence axes and peduncles were studied using light and scanning electron microscopy. Inflorescences are bractless spikes with flowers arranged in trimerous whorls. Except in the inflorescence tip (where the flower groundplan is variable), flowers possess two tepals in transversal‐abaxial positions, six stamens in two trimerous whorls and four carpels in median and transversal positions. Fruits are indehiscent. The shared possession of orthotropous ovules supports the molecular phylogenetic placement of Maundia as sister to a large clade including Potamogetonaceae and related families. Maundia and Aponogeton spp. share the same highly unusual floral groundplan, a homoplastic similarity that can be explained by spatial constraints in developing inflorescences. The nucellar coenocyte of Maundia appears to be unique among monocots. As Maundia exhibits a mosaic of features characteristic of other families of tepaloid core Alismatales, its segregation as a separate family is plausible. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 12–45.     

Comparative floral structure and systematics in Ochnaceae s.l. (Ochnaceae,Quiinaceae and Medusagynaceae; Malpighiales)

Ochnaceae s.l. (Ochnaceae, Quiinaceae and Medusagynaceae), one of the well‐supported subclades of the large order Malpighiales retrieved so far in molecular phylogenetic studies, were comparatively studied with regard to floral structure using microtome section series and scanning electron microscopy (SEM). Floral morphology, anatomy and histology also strongly reflect this close relationship. Potential synapomorphies of the subclade include: flowers nectarless, sepals of different sizes within a flower, petals not retarded in development and forming the protective organs of advanced floral buds, petal aestivation contort, petals with three vascular traces, petals reflexed over the sepals and directed toward the pedicel, polystemony, anthers almost or completely basifixed, gynoecium often with more than five carpels, short gynophore present, styles separate for at least their uppermost part and radiating outwards, suction‐cup‐shaped stigmas, vasculature forming a dorsal band of bundles in the upper stylar region, gynoecium epidermis with large, radially elongate cells, ovules either weakly crassinucellar or incompletely tenuinucellar with an endothelium, abundance of tanniferous tissues and sclerenchyma in floral organs. The most strongly supported subclade of two of the three families in molecular analyses, Quiinaceae and Medusagynaceae, is also particularly well supported by floral structural features, including the presence of functionally and morphologically unisexual flowers, a massive thecal septum that persists after anther dehiscence, styles radiating outward from the ovary, two lateral ovules per carpel, positioned one above the other, conspicuous longitudinal ribs on the ovary wall at anthesis, and a ‘false endothelium’ on the nucellus at anthesis. Additionally, the group fits well in Malpighiales and further emphasizes the relationship of Malpighiales with Celastrales and Oxalidales, and thus the unity of the COM clade. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 170 , 299–392.     

Comparative floral structure and systematics in Celastrales (Celastraceae, Parnassiaceae, Lepidobotryaceae)

Floral morphology, anatomy and histology in the newly circumscribed order Celastrales, comprising Celastraceae, Parnassiaceae and Lepidobotryaceae are studied comparatively. Several genera of Celastraceae and Lepidobotrys (Lepidobotryaceae) were studied for the first time in this respect. Celastraceae are well supported as a group by floral structure (including genera that were in separate families in earlier classifications); they have dorsally bulged‐up locules (and thus apical septa) and contain oxalate druses in their floral tissues. The group of Celastraceae and Parnassiaceae is also well supported. They share completely syncarpous gynoecia with commissural stigmatic lobes (and strong concomitant development of the commissural vascular bundles but weak median carpel bundles), only weakly crassinucellar or incompletely tenuinucellar ovules with an endothelium, partly fringed sepals and petals, protandry in bisexual flowers combined with herkogamy by the movement of stamens and anther abscission, and stamens fused with the ovary. In contrast, Lepidobotryaceae are more distant from the other two families, sharing only a handful of features with Celastraceae (not Parnassiaceae), such as pseudohermaphroditic flowers, united stamen bases forming a collar around the gynoecium and seeds with a conspicuous aril. However, all three families together are also somewhat supported as a group and share petals that are not retarded in late floral bud development, 3‐carpellate gynoecia, ventral slits of carpels closed by long interlocking epidermal cells and pollen tube transmitting tissue encompassing several cell layers, both integuments usually more than two cell layers thick, and only weak or lacking floral indumentum. In some molecular analyses Celastrales form an unsupported clade with Malpighiales and Oxalidales. This association is supported by floral structure, especially between Celastrales and Malpighiales. Among Celastrales, Lepidobotryaceae especially share special features with Malpighiales, including a diplostemonous androecium with ten fertile stamens, epitropous ovules with an obturator and strong vascularization around the chalaza. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149 , 129–194.     

Comparative floral structure and systematics in Rhizophoraceae,Erythroxylaceae and the potentially related Ctenolophonaceae,Linaceae, Irvingiaceae and Caryocaraceae (Malpighiales)

Within the rosid order Malpighiales, Rhizophoraceae and Erythroxylaceae (1) are strongly supported as sisters in molecular phylogenetic studies and possibly form a clade with either Ctenolophonaceae (2) or with Linaceae, Irvingiaceae and Caryocaraceae (less well supported) (3). In order to assess the validity of these relationships from a floral structural point of view, these families are comparatively studied for the first time in terms of their floral morphology, anatomy and histology. Overall floral structure reflects the molecular results quite well and Rhizophoraceae and Erythroxylaceae are well supported as closely related. Ctenolophonaceae share some unusual floral features (potential synapomorphies) with Rhizophoraceae and Erythroxylaceae. In contrast, Linaceae, Irvingiaceae and Caryocaraceae are not clearly supported as a clade, or as closely related to Rhizophoraceae and Erythroxylaceae, as their shared features are probably mainly symplesiomorphies at the level of Malpighiales or a (still undefined) larger subclade of Malpighales, rather than synapomorphies. Rhizophoraceae and Erythroxylaceae share (among other features) conduplicate petals enwrapping stamens in bud, antepetalous stamens longer than antesepalous ones, a nectariferous androecial tube with attachment of the two stamen whorls at different positions: one whorl on the rim, the other below the rim of the tube, the ovary shortly and abruptly dorsally bulged and the presence of a layer of idioblasts (laticifers?) in the sepals and ovaries. Ctenolophonaceae share with Rhizophoraceae and/or Erythroxylaceae (among other features) sepals with less than three vascular traces, a short androgynophore, an ovary septum thin and severed or completely disintegrating during development, leading to a developmentally secondarily unilocular ovary, a zigzag‐shaped micropyle and seeds with an aril. Special features occurring in families of all three groupings studied here are, for example, synsepaly, petals not retarded and thus forming protective organs in floral bud, petals postgenitally fused or hooked together in bud, androecial tube and petals fusing above floral base, androecial corona, apocarpous unifacial styles, nucellus thin and long, early disintegrating (before embryo sac is mature), and nectaries on the androecial tube. Some of these features may be synapomorphies for the entire group, if it forms a supported clade in future molecular studies, or for subgroups thereof. Others may be plesiomorphies, as they also occur in other Malpighiales or also in Celastrales or Oxalidales (COM clade). The occurrence of these features within the COM clade is also discussed. © 2011 The Linnean Society of London, Botanical Journal of the Linnean Society, 2011, 166 , 331–416.     

Comparative floral structure and systematics in Oxalidales (Oxalidaceae, Connaraceae, Brunelliaceae, Cephalotaceae, Cunoniaceae, Elaeocarpaceae, Tremandraceae)

Floral morphology, anatomy and histology were studied in representatives of all families of current Oxalidales, which were recently constituted as a result of molecular systematic studies by other authors, and are composed of families of different positions in traditional classifications (Oxalidaceae, Connaraceae, Brunelliaceae, Cephalotaceae, Cunoniaceae, Elaeocarpaceae, Tremandraceae). Two of the three pairs of sister (or nested) families that come out in molecular analyses are highly supported by floral structure: Oxalidaceae/Connaraceae and Elaeocarpaceae/Tremandraceae, whereas Cephalotaceae/Cunoniaceae are not especially similar at the level of Oxalidales. Oxalidaceae and Connaraceae share petals that are postgenitally united into a basal tube (although they are imbricate in both) but free at the insertion zone, stamens that are congenitally united at the base, uniseriate glandular hairs on the stamen filaments, and ovules that are hemianatropous to almost orthotropous. The sharing of a special type of sieve-tube plastids and of trimorphic heterostyly, studied by other authors, should also be mentioned. With Brunelliaceae, the two families share an androgynophore and nectaries at the base of the stamens in alternisepalous sectors. Elaeocarpaceae and Tremandraceae share buzz-pollinated flowers and a syndrome of features functionally connected with it. In addition, petals are larger than sepals in advanced bud, they are valvate, involute and enwrap part of the adjacent stamens, they have three vascular traces. Lignified hairs are common on the anthers and are found in the ovary locules and on the ovules (not lignified) of representatives of both families. Ovules have a chalazal appendage, and the inner integument is much thicker than the outer.  © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society , 2002, 140 , 321–381.     

Comparative floral morphology and anatomy of Anacardiaceae and Burseraceae (Sapindales), with a special focus on gynoecium structure and evolution

Anacardiaceae and Burseraceae are traditionally distinguished by the number of ovules (1 vs. 2) per locule and the direction of ovule curvature (syntropous vs. antitropous). Recent molecular phylogenetic studies have shown that these families are sister groups in Sapindales after having been separated in different orders for a long time. We present a comparative morphological study of the flower structure in both families. The major clades, usually supported in molecular phylogenetic analyses, are well supported by floral structure. In Anacardiaceae, there is a tendency to gynoecium reduction to a single fertile carpel (particularly in Anacardioideae). The single ovule has a long and unusually differentiated funicle, which connects with the stylar pollen tube transmitting tract in all representatives studied. In Anacardiaceae–Spondiadoideae, there is a tendency to form an extensive synascidiate zone, with a massive remnant of the floral apex in the centre; these features are also present in Beiselia (Burseraceae) and Kirkiaceae (sister to Anacardiaceae plus Burseraceae) and may represent a synapomorphy or apomorphic tendency for the three families. In core Burseraceae, gynoecium structure is much less diverse than in Anacardiaceae and has probably retained more plesiomorphies. Differences in proportions of parts of the ovules in Anacardiaceae and Burseraceae are linked with the different direction of ovule curvature. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159 , 499–571.     

Comparative floral structure and systematics of the clade of Lophopyxidaceae and Putranjivaceae (Malpighiales)

In molecular phylogenetic studies, Lophopyxidaceae and Putranjivaceae are well supported as sisters in the large rosid order Malpighiales. As the floral structure of both families is poorly known and the two families have never been compared, the present comparative study was carried out, as part of a larger project on the comparative floral structure of Malpighiales, using microtome section series and scanning electron microscopy (SEM) studies. Similar to other angiosperm clades, it appears that the structure of the ovules is a strong marker for suprafamilial relationships in Malpighiales. Both families have two collateral pendant antitropous ovules per carpel associated with obturators (as in some Euphorbiaceae s.l., to which Putranjivaceae belonged in earlier classifications). However, in contrast with Euphorbiaceae s.l., the ovules are not crassinucellar, but either incompletely tenuinucellar or only weakly crassinucellar with a long and conspicuously slender nucellus and an endothelium, and do not have a nucellar beak, but a normal micropyle, features they share with families other than Euphorbiaceae s.l. among Malpighiales. Other shared features of the two families include the following. The outer sepals tend to be smaller than the inner ones and the sepals do not protect the gynoecium in older buds. Sepals of some taxa have a single vascular trace. A short zone of synsepaly tends to be present. Stamens tend to be antesepalous in haplostemonous flowers. A short gynophore is present. The synascidiate zone extends up to above the placenta, but is restricted to the ovary in taxa with more than one carpel. The micropyle is formed by the inner integument. The ventral carpel slits extend down into the synascidiate zone as postgenitally fused furrows. The carpels have a broad dorsal band of vascular bundles in the style. The overall floral structure of the two families corroborates their sister position well and does not support the earlier association of Putranjivaceae with Euphorbiaceae s.l. or of Lophopyxidaceae with Geraniales–Sapindales–Celastrales, which rely on shared superficial floral similarities. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 172 , 404–448.     

First steps towards a floral structural characterization of the major rosid subclades

A survey of our own comparative studies on several larger clades of rosids and over 1400 original publications on rosid flowers shows that floral structural features support to various degrees the supraordinal relationships in rosids proposed by molecular phylogenetic studies. However, as many apparent relationships are not yet well resolved, the structural support also remains tentative. Some of the features that turned out to be of interest in the present study had not previously been considered in earlier supraordinal studies. The strongest floral structural support is for malvids (Brassicales, Malvales, Sapindales), which reflects the strong support of phylogenetic analyses. Somewhat less structurally supported are the COM (Celastrales, Oxalidales, Malpighiales) and the nitrogen-fixing (Cucurbitales, Fagales, Fabales, Rosales) clades of fabids, which are both also only weakly supported in phylogenetic analyses. The sister pairs, Cucurbitales plus Fagales, and Malvales plus Sapindales, are structurally only weakly supported, and for the entire fabids there is no clear support by the present floral structural data. However, an additional grouping, the COM clade plus malvids, shares some interesting features but does not appear as a clade in phylogenetic analyses. Thus it appears that the deepest split within eurosids–that between fabids and malvids - in molecular phylogenetic analyses (however weakly supported) is not matched by the present structural data. Features of ovules including thickness of integuments, thickness of nucellus, and degree of ovular curvature, appear to be especially interesting for higher level relationships and should be further explored. Although features of interest are not necessarily stable at the level of a large clade, they do show a considerable concentration in particular clades and are rare or lacking in others. This may be viewed as a special trend for this feature to evolve in this group or to be conserved as a synapomorphy (or a combination of both).     

Comparative floral structure and systematics in Cucurbitales (Corynocarpaceae, Coriariaceae, Tetramelaceae, Datiscaceae, Begoniaceae, Cucurbitaceae, Anisophylleaceae)

Floral structure, including morphology, anatomy and histology, was comparatively studied in representatives of all seven families of Cucurbitales as currently circumscribed by other authors based on molecular analyses and including Corynocarpaceae, Coriariaceae, Tetramelaceae, Datiscaceae, Begoniaceae, Cucurbitaceae and Anisophylleaceae. Three superfamilial clades are supported by floral structure: Tetramelaceae/Datiscaceae, Tetramelaceae/Datiscaceae/Begoniaceae and Corynocarpaceae/Coriariaceae. Anisophylleaceae appear most isolated in Cucurbitales, and show more similarities with Oxalidales, especially Cunoniaceae, although some features of interest are shared with other Cucurbitales and not Oxalidales. Tetramelaceae and Datiscaceae share dioecy, completely isomerous (but not regularly pentamerous) flowers (not in male Datiscaceae), only small sepals, lacking petals (not in male Octomeles). Tetramelaceae, Datiscaceae and Begoniaceae share the presence of numerous small ovules and seeds with a large‐celled surface, 2‐cell‐layered integuments, and a collar around the funicle by an extension of the outer integument. Corynocarpaceae and Coriariaceae share thick petals, unifacial stigmas, superior ovaries with a single, median, pendant syntropous ovule per carpel, and annular outer integuments with vasculature at the base. The four classical core families of Cucurbitales: Tetramelaceae, Datiscaceae, Begoniaceae and Cucurbitaceae (relationship unresolved, not retrieved as a clade as yet in molecular studies) share in various combinations androdioecy, basifixed and extrorse or latrorse anthers, trimerous gynoecia, bifurcate free carpel parts, an extended roof over the ovary formed by the ventral parts of the carpels, and parietal placentae. Trends of interest at the order level are unisexual flowers, thick, pointed petals (if present) that do not conform to the model in other rosids or basal core eudicots, a 2‐cell‐layered inner integument, which is delayed in development, and lacking or scant tanniferous tissues in flowers. © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society, 2004, 145 , 129–185.     

Glandulocalyx upatoiensis, a fossil flower of Ericales (Actinidiaceae/Clethraceae) from the Late Cretaceous (Santonian) of Georgia, USA

Background and Aims

Ericales are a major group of extant asterid angiosperms that are well represented in the Late Cretaceous fossil record, mainly by flowers, fruits and seeds. Exceptionally well preserved fossil flowers, here described as Glandulocalyx upatoiensis gen. & sp. nov., from the Santonian of Georgia, USA, yield new detailed evidence of floral structure in one of these early members of Ericales and provide a secure basis for comparison with extant taxa.

Methods

The floral structure of several fossil specimens was studied by scanning electron microscopy (SEM), light microscopy of microtome thin sections and synchrotron-radiation X-ray tomographic microscopy (SRXTM). For direct comparisons with flowers of extant Ericales, selected floral features of Actinidiaceae and Clethraceae were studied with SEM.

Key Results

Flowers of G. upatoiensis have five sepals with quincuncial aestivation, five free petals with quincuncial aestivation, 20–28 stamens arranged in a single series, extrorse anther orientation in the bud, ventral anther attachment and a tricarpellate, syncarpous ovary with three free styles and numerous small ovules on axile, protruding-diffuse and pendant placentae. The calyx is characterized by a conspicuous indumentum of large, densely arranged, multicellular and possibly glandular trichomes.

Conclusions

Comparison with extant taxa provides clear evidence for a relationship with core Ericales comprised of the extant families Actinidiaceae, Roridulaceae, Sarraceniaceae, Clethraceae, Cyrillaceae and Ericaceae. Within this group, the most marked similarities are with extant Actinidiaceae and, to a lesser degree, with Clethraceae. More detailed analyses of the relationships of Glandulocalyx and other Ericales from the Late Cretaceous will require an improved understanding of the morphological features that diagnose particular extant groups defined on the basis of molecular data.     

Development of the floral shoot and pre‐anthesis cleistogamy in Hydrobryopsis sessilis (Podostemaceae)

The reproductive biology of Hydrobryopsis sessilis (Podostemaceae, subfamily Podostemoideae), a reduced, threatened, aquatic angiosperm endemic to the Western Ghats of India, was examined. This is the first report on the transition from the vegetative to the reproductive phase in this plant, describing floral ontogeny, pollination and the breeding system. The cytohistological zonation of the apical meristem of the reproductive thallus is identical to that of the apical meristem of the vegetative thallus. The floral shoots do not replace vegetative shoots (i.e. the vegetative shoots never bear flowers), but form at new sites at the tip of the flattened plant body. Each floral shoot meristem is tiny, deep‐seated and concave and arises endogenously following lysigeny. The floral shoot meristem gives rise to four to six bracts in a distichous manner. The development of spathe, stamens and carpels is described. The ab initio dorsiventrality of the carpels and the occurrence of endothelium in the ovules are reported. The mature stigmas and anthers lie close to each other. The pollen germinates within undehisced anthers and the pollen tubes enter the stigmas in the unopened floral bud, leading to pre‐anthesis, complete, constitutional cleistogamy under water. The seed set is 63.2%. A significant finding is the penetration of several pollen tubes into the filaments of stamens in 16% of the flower buds, indicating a trend towards cryptic self‐fertilization. The Indian Podostemoideae appear to show a shift from xenogamy or geitonogamy or autogamy in a chasmogamous flower to complete autogamy in a cleistogamous flower. The floral modifications leading to cleistogamy in H. sessilis have been identified. © 2009 The Linnean Society of London, Botanical Journal of the Linnean Society, 2009, 159 , 222–236.     

The morphology and relationships of the Sphaerosepalaceae (Malvales)

The comparative vegetative and reproductive morphology and anatomy of the Malagasy endemic family Sphaerosepalaceae is examined in light of two current competing hypotheses of relationship from recent molecular studies. Sphaerosepalaceae are similar to Thymelaeaceae on the basis of leaf architecture, calyx vasculature and in having endostomal micropyles. Comparisons with Tepuianthus and Thymelaeaceae subfamily Octolepidoideae are drawn on the basis of seed structure, indument type, perianth structure and pollen. Resin-filled, sclerenchymatous idioblasts, floral (positional) monosymmetry, a single series of stamen trunk bundles and a well-developed bixoid chalaza in the seed of Dialyceras parvifolium link Sphaerosepalaceae with its other putative sister group: a clade containing Bixaceae, Cochlospermaceae and Diegodendraceae. Synapomorphies of Sphaerosepalaceae include: fused, intrapetiolar stipules, embryo structure, pollen with endoapertures encompassing the ectoapertures and a tetramerous perianth. The extremely well-developed apical septum in the eusyncarpous gynoecium of Rhopalocarpus suggests that the gynoterminal style present in this genus has been secondarily derived from an ancestor with a fully syncarpous, basistylous gynoecium, as in Dialyceras . The morphological and evolutionary nature of basistylous and apically septate gynoecia is discussed. A rosette arrangement of ovules in each carpel coccus of D. coriaceum expands the bauplan concept of Sphaerosepalaceae and is probably unique among angiosperms as a whole.  © 2004 The Linnean Society of London, Botanical Journal of the Linnean Society , 2004, 144 , 1–40.