Floral structure and evolution of primitive angiosperms: Recent advances

Concepts of primitive angiosperm flowers have changed in recent years due to new studies on relic archaic groups, new paleobotanical finds and the addition of molecular biological techniques to the study of angiosperm systematics and evolution.Magnoliidae are still the hot group, but emphasis is now on small primitive flowers with few organs and also on the great lability of organ number. Of the extant groups, a potential basal position of the paleoherbs has been discussed by some authors. Although some paleoherbs have a simple gynoecium with a single orthotropous ovule, anatropous ovules may still be seen as plesiomorphic in angiosperms. Anatropy is not necessarily a consequence of the advent of closed carpels. It may also exhibit biological advantages under other circumstances as is the case in podocarps among gymnosperms. Valvate anthers have now been found in most larger subgroups of theMagnoliidae (recently also in paleoherbs) and in some Cretaceous fossils. Nevertheless, as seen from its systematic distribution, valvate dehiscence is not necessarily plesiomorphic for the angiosperms, but may be a facultative by-product of the thick connectives and comparatively undifferentiated anther shape inMagnoliidae and lowerHamamelididae. A perianth is relatively simple in extantMagnoliidae or even wanting in some families. In groups with naked flowers the perianth may have been easily lost because integration in the floral architecture was less pronounced than in more advanced angiosperm groups. Problems with the comparison of paleoherb flowers with those ofGnetales are discussed. The rapid growth of information from paleobotany and molecular systematics requires an especially open attitude towards the evaluation of various hypotheses on early flower evolution in the coming years.     

Normapolles plants: a prominent component of the Cretaceous rosid diversification

The Normapolles complex, characterised by its oblate and triaperturate pollen, constitutes an important and diverse element of many Late Cretaceous and Early Cainozoic floras of the Northern Hemisphere. Based on the dispersed pollen record alone it has been difficult to assess systematic affinities, but relationships with Fagales have been proposed. Over the past twenty years several exquisitely preserved Late Cretaceous reproductive structures with Normapolles type pollen in situ have been described. In this study we provide a summary and new information of these floral structures. Further, a new genus, Dahlgrenianthus, is described from the Late Cretaceous of southern Sweden. The genus includes the type species Dahlgrenianthus suecicus, a number of reproductive structures referred to Dahlgrenianthus sp., and Dahlgrenianthus trigonus (Knobloch et Mai) comb. nov. from the Maastrichtian flora of Walbeck, Germany. Dahlgrenianthus comprises small flowers with pentamerous perianth and androecium and a tricarpellate gynoecium. It is distinguished from all other Normapolles floral structures in its hypogynous floral organisation. All Normapolles floral structures described so far are thought to be related to various members of the core Fagales, but the group is obviously not monophyletic. The stratigraphic range of the Normapolles taxa and other fagalean fossils strongly suggests that all major fagalean lineages were present by the Cenomanian or earlier.     

Comparative floral anatomy and ontogeny in Magnoliaceae

Floral anatomy and ontogeny are described in six species of Magnoliaceae, representing the two subfamilies Liriodendroideae (Liriodendron chinese and L. tulipifera) and Magnolioideae, including species with terminal flowers (Magnolia championi, M. delavayi, M. grandiflora, M. paenetalauma) and axillary flowers (Michelia crassipes). The sequence of initiation of floral organs is from proximal to distal. The three distinct outermost organs are initiated in sequence, but ultimately form a single whorl; thus their ontogeny is consistent with a tepal interpretation. Tepals are initiated in whorls, and the stamens and carpels are spirally arranged, though the androecium shows some intermediacy between a spiral and whorled arrangement. Carpels are entirely free from each other both at primordial stages and maturity. Ventral closure of the style ranges from open in Magnolia species examined to partially closed in Michelia crassipes and completely closed in Liriodendron, resulting in a reduced stigma surface. Thick-walled cells and tannins are present in all species except Michelia crassipes. Oil cells are normally present. Floral structure is relatively homogeneous in this family, although Liriodendron differs from other Magnoliaceae in that the carpels are entirely closed at maturity, resulting in a relatively small stigma, in contrast to the elongate stigma of most species of Magnolia. The flower of Magnolia does not terminate in an organ or organ whorl but achieves determinacy by gradual diminution.     

Distyly and heteromorphic incompatibility in oceanic island species ofErythroxylum (Erythroxylaceae)

Surveys of oceanic island floras have shown that heterostyly is usually absent in such regions, probably because this floral polymorphism is often associated with a self-incompatibility system. In this context we describe the floral biology of three species ofErythroxylum on La Réunion island and examine the compatibility relationships of one of these species,E. laurifolium. All three species are distylous but differ in relative stigma-anther separation in the different morphs. In general, short-styled flowers have greater stigma-anther separation than long-styled flowers, which are often homostylous in appearance. This lack of stigma-anther separation in long-styled flowers is due to style twisting which improves reciprocity at the high organ level. The reduced stigma-anther separation does not appear to be associated with the evolution of selfing asErythroxylum laurifolium shows heteromorphic self-incompatibility. The presence of heteromorphic incompatibility in a group of species that have colonized an oceanic island is discussed.     

Reproductive ecology of the Qinghai-Tibet Plateau endemic Gentiana straminea (Gentianaceae), a hermaphrodite perennial characterized by herkogamy and dichogamy

The combined occurrence of both herkogamy and dichogamy in a hermaphrodite species has been considered to strongly favour outcrossing. In this study, we investigated in detail the reproductive ecology of Gentiana straminea Maxim. (Gentianaceae), a hermaphrodite perennial endemic to the Qinghai-Tibet Plateau. In a series of observations and experiments over four consecutive years, we examined whether the combination of dichogamy and herkogamy in individual flowers completely prevents geitonogamous pollen transfer in this species. The mode of floral development clearly indicates that autonomous self-pollination is completely avoided through herkogamy and dichogamy in individual flowers. This implication was confirmed by the breeding experiments, since no seed was produced when flowers were isolated. However, this gentian proved to be highly self-compatible when geitonogamous selfing was artificially induced. Many flowers opened simultaneously on individual plants, the ratio of male to female phase flowers was close to 2:1 in each inflorescence at the full anthesis phase, and they were randomly distributed amongst the upper, middle and lower parts of each stem's inflorescence. On average, Bombus sushikini Skorikov, the most frequent visitor and only legitimate pollinator of G. straminea, visited nearly two flowers per inflorescence, and four flowers per plant. Among the pollinators' foraging bouts, the proportions of geitonogamous visits to inflorescences or flowers within an individual plant were 29% and 37%, respectively. Therefore, despite the strict dichogamous and herkogamous characteristics of the individual flowers, geitonogamous selfing might still prevail in G. straminea because of the size of its floral displays and the continuous visiting behavior of B. sushkini.     

Developmental morphology of branching flowers in Nymphaea prolifera

Nymphaea and Nuphar (Nymphaeaceae) share an extra-axillary mode of floral inception in the shoot apical meristem (SAM). Some leaf sites along the ontogenetic spiral are occupied by floral primordia lacking a subtending bract. This pattern of flower initiation in leaf sites is repeated inside branching flowers of Nymphaea prolifera (Central and South America). Instead of fertile flowers this species usually produces sterile tuberiferous flowers that act as vegetative propagules. N. prolifera changes the meristem identity from reproductive to vegetative or vice versa repeatedly. Each branching flower first produces some perianth-like leaves, then it switches back to the vegetative meristem identity of the SAM with the formation of foliage leaves and another set of branching flowers. This process is repeated up to three times giving rise to more than 100 vegetative propagules. The developmental morphology of the branching flowers of N. prolifera is described using both microtome sections and scanning electron microscopy.     

Sequence evolution and sex-specific expression patterns of the C class floral identity gene, <Emphasis Type="Italic">SpAGAMOUS</Emphasis>, in dioecious <Emphasis Type="Italic">Spinacia oleracea</Emphasis> L

Development in dioecious cultivated spinach, Spinacia oleracea, is distinguished by the absence of alternative reproductive organ primordia in male and female flowers. Given the highly derived floral developmental program in spinach, we wished to characterize a spinach C class floral identity gene and to determine the patterns of sequence evolution as well as compare the spatial and temporal expression patterns with those of AGAMOUS. The isolated cDNA sequence clusters phylogenetically within the AGAMOUS/FARINELLI C class clade. In comparison with the SLM1 sequence from the related Silene latifolia, amino acid replacements are highly conservative and non-randomly distributed, being predominantly found in hinge regions or on exposed surfaces of helices. The spinach gene (SpAGAMOUS) appears to be exclusively expressed in reproductive tissues and not in vegetative organs. Initial expression of SpAGAMOUS is similar in male and female floral primordia. However, upon initiation of the first whorl organs, SpAGAMOUS becomes restricted to meristemic regions from which the reproductive primordia will develop. This results in an early gender-specific pattern. Thus, the spinach C class gene is differentially expressed prior to reproductive organ development and is, at least, correlated with, if not directly involved in, the sexual dimorphism in spinach.Electronic Supplementary Material Supplementary material is available for this article at     

Floral sex ratio variation in hermaphrodites of gynodioeciousChionographis japonica var.kurohimensis Ajima et Satomi (Liliaceae)

Intrapopulation and interpopulation variations in floral sex ratio in hermaphrodites of gynodioeciousChionographis japonica var.kurohimensis (Liliaceae) were examined. The relative ratio of male flowers to total flowers (male and perfect flowers) decreased with plant size, suggesting size-dependent gender modification. The relative ratio of male flowers per population-basis is negatively correlated with the mean number of perfect flowers. Since the number of perfect flowers proportionally increased with plant size, populations showing low maleness consist of relatively bigger plants and are considered to be in high-quality environment. On the other hand, the relative ratio of male flowers per population basis is independent of female frequency in the population. Plasticity in gender expression probably plays an important role of maintenance of gynodioecy inC. japonica var.kurohimensis.     

Aspects of evolutionary differentiation of theHamamelidaceae and the LowerHamamelididae

New investigations on the flower and fruit structure of extantHamamelidaceae and other LowerHamamelididae together with new finds of fossil flowers and seeds from the Upper and Lower Cretaceous provide the outline of an increasingly more differentiated picture of the early evolution of the subclass. Three patterns of valvate anther dehiscence are recognized in the subfamilyHamamelidoideae (and the subclassHamamelididae). The basic (plesiomorphic) type within theHamamelididae has 2 valves per theca. The type with 1 valve but 2 pollen sacs per theca is both consistent and exclusive for the 5 southern genera of theHamamelidaceae. They seem to be the remnants of a homogeneous group that originated before the Upper Cretaceous. This is supported by fossil hamamelidaceous flowers from the Upper Cretaceous that have thecae with 1 valve. Since several-seededHamamelidaceae predate one-seeded forms in the fossil seed record (in Europe) and the systematic structure of the one-seeded group is relatively more homogeneous, several-seeded groups are considered to be more ancient. Several parallel evolutionary trends are recognized within theHamamelidaceae as well as within the LowerHamamelididae: anther dehiscence with 2 valves per theca 1 slit or 1 valve; pollen sacs per theca 2 1; pollen tricolpate polyforate; exine coarsely reticulate finely reticulate; loss of perianth (tepals or petals and sepals) and concomitant loss of fixed number of floral organs; differentiation of exposed nectaries.     

Über sphingophile Angiospermen Brasiliens

In order to study the functional differentiation in flowers of 15 sphingophilous Brazilian Angiosperms, anthesis, flower morphology, flower odours and the behaviour of visiting animals were investigated. All 15 species were found to have nocturnal anthesis, but only 13 proved to be predominantly visited by hawk-moths. Of the 3Lafoensia populations studied, one was pollinated only by hawk-moths, one was chiropterophilous and one had a mixed bat-moth pollination; there are corresponding differences in flower dimensions.

Unserem verehrten Lehrer, dem kürzlich tragisch verstorbenen Univ.-Prof. Dr.Felix J. Widder, Graz, in Dankbarkeit gewidmet.     

Floral structure and ontogeny in Globba (Zingiberaceae)

We present new comparative morphological and ontogenetic data on flowers and bulbils of Globba (Zingiberaceae) to clarify their homologies. Globba flowers are characteristically Zingiberaceous, possessing a single stamen and epigynous (``supragynopleural') nectaries, but are unusual as the anther bears triangular lateral outgrowths and the style is held tightly in position across the curvature of the filament like a bowstring. Floral ontogeny in Globba is similar to other Zingiberaceae. Characteristic features, such as anther wings, occur late in development, shortly before anthesis. Unusually Globba has zygomorphic style anatomy with only two abaxial vascular bundles, in contrast to most other Zingiberaceae, which possess three stylar traces. The ovary is unilocular and lacks septa. Bulbils have enclosing bracts and replace flowers in the lower part of the inflorescence; they consist of a shoot with an enlarged corky storage root forming the bulk of the propagule.     

Estimates of hierarchical variation in flower morphology in natural populations ofScleranthus annuus (Caryophyllaceae), an inbreeding annual

The variation in two sets of morphological characters of the flowers of the highly inbreedingScleranthus annuus (Caryophyllaceae) was assessed using 15–20 plants from each of 20 natural populations from the southernmost region of Sweden. The stamen fertility data set consisted of 10 characters describing the degree of fertility of the ten stamens/staminoids, while the sepal/gynoecium data set comprised 10 sepal characters, together with style and stigma length. Substantial variation was found in both the degree of development and the fertility of the stamens, the degree of variability in stamen fertility being related to stamen position within the flower. Considerable variation was found in the characters of the sepal and the gynoecium. Hierarchical analyses of variance indicated that 29% of the variation in total male reproductive effort was distributed among populations, 28% among plants within populations and 43% represented within-plant variation. The corresponding averages for the characters from the sepal/gynoecium data set are 26, 38, and 35%: a greater proportion of the total variance in female reproductive characters is accounted for by among individual variation than is the case with the male reproductive characters. Significance tests of Mahalanobis distances derived by canonical variate analyses indicated that all populations were significantly separated using the sepal/gynoecium data set, while only 50% of the pairwise comparisons on the basis of the stamen fertility data set were significant. Cluster analysis did not reveal any aggregation of the populations. The incongruence of the two data sets and their ability to discriminate between the populations is discussed.     

Solar furnaces or swamp coolers: costs and benefits of water use by solar-tracking flowers of the alpine snow buttercup, Ranunculus adoneus

Solar tracking or heliotropism simultaneously raises organ temperature and light interception. For leaves and flowers carbon gain is maximized at the expense of water loss. In this study I explore how costs and benefits associated with water use by solar-tracking flowers of the alpine snow buttercup, Ranunculus adoneus change with ambient temperature. First, I test whether heliotropism increases the water cost of reproduction in the snow buttercup under extant alpine conditions. I then explore whether water use for evaporative cooling in solar-tracking flowers reduces the risk of over-heating as temperatures increase. Solar tracking, by elevating floral temperature and irradiance causes a 29% increase in water uptake by flowers. Gas exchange measurements suggest that the extra water taken up by solar-tracking flowers is released through transpiration. Transpirational cooling in turn allows solar-tracking flowers to gain advantages of enhanced light interception and warmth while reducing the risk of over-heating. Transpiration reduces excess temperature in solar-tracking flowers, but at a water cost. Results show that even in cool alpine habitats, flower heliotropism has water costs to balance its reproductive advantages. Plants with solar-tracking flowers may tolerate hotter conditions if soil moisture is plentiful, but not under drought.     

Developmental analyses reveal early arrests of the spore-bearing parts of reproductive organs in unisexual flowers of cucumber (<Emphasis Type="Italic">Cucumis sativus</Emphasis> L.)

To understand the regulatory mechanisms governing unisexual flower development in cucumber, we conducted a systematic morphogenetic analysis of male and female flower development, examined the dynamic changes in expression of the C-class floral organ identity gene CUM1, and assessed the extent of DNA damage in inappropriate carpels of male flowers. Accordingly, based on the occurrence of distinct morphological events, we divided the floral development into 12 stages ranging from floral meristem initiation to anthesis. As a result of our investigation we found that the arrest of stamen development in female flowers, which occurs just after the differentiation between the anther and filament, is mainly restricted to the primordial anther, and that it is coincident with down-regulation of CUM1 gene expression. In contrast, the arrest of carpel development in the male flowers occurs prior to the differentiation between the stigma and ovary, given that no indication of ovary differentiation was observed even though CUM1 gene expression remained detectable throughout the development of the stigma-like structures. Although the male and female reproductive organs have distinctive characteristics in terms of organ differentiation, there are two common features regarding organ arrest. The first is that the arrest of the inappropriate organ does not affect the entirety of the organ uniformly but occurs only in portions of the organs. The second feature is that all the arrested portions in both reproductive organs are spore-bearing parts.Abbreviations SEM Scanning electron microscopy - TEM Transmission electron microscopy - TUNEL TdT-mediated dUTP nick-end labeling     

Floral biology of Nuphar pumila (Timm) DC. (Nymphaeaceae) in China

Anthesis in individual flowers of Nuphar pumila (Timm) DC. occurs for four consecutive days. First-day flowers are protogynous and functionally female. Flowers can open completely on the first day of anthesis. This contrasts with all previous reports, which state that first-day flowers of Nuphar are characterized by partial expansion of the calyx, leaving a distal small triangular opening just above the stigmatic disc. Flowers close completely on the first night of anthesis and remain partially open on the subsequent three nights. During the entire anthesis period the stigmas emit a sweet, fruity odor and the petal nectaries produce visible nectar drops. The stigma of N. pumila is secretory and unicellular-papillate. Pollen grains are monosulcate with long spines. Our observations on the mating system of N. pumila indicate that neither asexual seed production nor spontaneous self-pollination occurs. Cross-pollination of second-, third- and fourth-day flowers produced few seeds. Flowers of N. pumila were mainly pollinated by sweat bees, with flies playing a minor pollination role. No beetle visits were observed. Our insect-pollination observations substantiate the view that the relative contribution of flies, bees, and beetles to pollination in a single Nuphar population depends on two factors: the relative abundance of the insects, and presence of alternative food sources.     

Intraspecific Variation of Floral Scent Chemistry in Magnolia kobus DC. (Magnoliaceae)

Magnolia kobus was examined at 32 sites in Japan (109 female-stage flowers from 52 plants) by GC-MS. Major chemical compounds (a total of 36 chemicals) emitted from the flowers were: linalool (and its oxides), limonene, cis- and trans-β-Ocimene, benzaldehyde, benzyl alcohol, benzyl cyanide, and 2-aminobenzaldehyde. Linalool and its oxides were the most abundant components of floral scents in 21 individuals. The rate at which chemical volatiles were emitted ranged from 0.002 to 0.929 μg/flower/hour (average 0.211). High quantitative and qualitative variation in floral scent chemistry among individuals was found throughout the range of M. kobus, especially in central Honshu. The high variability in floral scent chemistry may be due to the importance of visual cues in the reproductive biology of M. kobus which flowers in early spring, resulting in decreased selection for specific floral scent profiles. Alternatively, different scent compounds or chemical profiles may be equally effective in attracting pollinators. Received 25 June 2001/ Accepted in revised form 25 August 2001     

A comparative floral and pollination biology ofTricyrtis flava maxim.,T. nana yatabe andT. ohsumiensis

The floral and pollination biology of three closely related species,Tricyrtis flava, T. nana andT. ohsumiensis, were comparatively investigated. The primary pollinator wasBombus diversus in all the three species observed, andAmegilla sp. also acted forT. ohsumiensis. The flowers ofT. flava andT. ohsumiensis bloom for two days and are protandrous. Thus autogramy seems to be prevented in these species when the larger bees forage on them, though geitonogamy may also occur. On the other hand,T. nana appears to be a primarily self-pollinating species. The flowers of this species open only during one day and are homogamy. The stigmata seem to receive much pollen of their own flower by the visit of bumblebees. Moreover, many flowers ofT. nana fruited without any visit of pollinators.T. nana has many features characterizing the autogamous derivatives.     

Expression analysis and genetic mapping of three <Emphasis Type="Italic">SEPALLATA</Emphasis>-like genes from peach (<Emphasis Type="Italic">Prunus persica</Emphasis> (L.) Batsch)

SEPALLATA (SEP) MADS box genes play essential and diverse roles in reproductive organ development. To investigate the SEP gene function in peach we isolated three SEP-like genes, PrpMADS2, PrpMADS5, and PrpMADS7, which belong to distinct SEP gene clades. They appeared as single copy genes in the peach genome and were found to preferentially express in flowers and fruits. Arabidopsis transformants expressing 35S: PrpMADS2 were indistinguishable from wild-type plants. Overexpression of PrpMADS5 led to earlier flowering. Through chimeric repressor silencing technology, PrpMADS5 was found to function in floral organ development. Expression of PrpMADS7 in Arabidopsis caused a dramatic attenuation of both juvenile and adult growth phases and, in severely affected plants, it led to flower formation immediately after the embryonic phase. Two microsatellite markers were developed for PrpMADS2 and PrpMADS5 and assigned to the genetic linkage groups 5 and 1, respectively. PrpMADS7, previously identified as PrpAGL2, and PrpMADS5 were identified as potential loci to modify the flowering time and floral organs in Prunus species. Moreover, our results showed the diversification of SEP genes in peach. The gene sequences have been deposited in GenBank and will appear under the accession numbers BQ102369, EF440351, and EF440352.     

Floral development in Adonideae (Ranunculaceae)

Floral development and floral phyllotaxis in species of Adonis, Callianthemum, and Trollius (Ranunculaceae) were studied with scanning electron microscopy. The floral organs are initiated in spiral sequence and the flowers have spiral phyllotaxis. The sepal primordia are broad, crescent-shaped, and truncate, but those of petals, stamens, and carpels are rather hemispherical. A relatively long plastochron appears to be present between the last sepal and the first petal as compared with the short and equal plastochrones of all subsequent floral organs. Maturation of the stamens within the androecium appears to be centripetal. The carpels have a short ascidiate zone. Placentation is uniformly lateral, even in Adonis and Callianthemum, which have only one fertile ovule per carpel (versus median in other genera of Ranunculoideae with a single fertile ovule). In Adonis and Callianthemum at the tip of the carpel the ventral slit is gaping and the stigma is broadly exposed, whereas in Trollius the stigma is narrower and more pronouncedly decurrent along the ventral slit. The petals in Callianthemum and Trollius are more conspicuously delayed in development than those in Adonis as compared with sepals and stamens. A short carpel stipe is formed early in Callianthemum but later in Adonis and Trollius. In Trollius farreri (commonly having only five carpels in contrast to other species of Trollius) the carpels form a single (spiral) series. Thus floral development is similar in all three genera and, at a lower level, Adonis and Callianthemum are especially close but have different autapomorphies, which reflects the current classification of the genera.     

Paleobotanical evidence on the early radiation of nonmagnoliid dicotyledons

Paleobotanical studies indicate that several isolated and systematically depauperate groups of extant woody dicotyledons originated in the Mid Cretaceous. TheChloranthaceae had probably differentiated into insect-pollinated (Chloranthus andSarcandra) and wind-pollinated (Ascarina andHedyosmum) forms by the end of the Albian, and leaves referable to theTrochodendrales are known from the Albian and Cenomanian. In the latest Cretaceous and Early Tertiary, extinct representatives of theTrochodendrales includedNordenskioldia and theJoffrea-Nyssidium complex. ThePlatanaceae also differentiated before the end of the Albian and initially had insect-pollinated, unisexual flowers with five carpels or stamens. Some of these features persisted in the platanoid lineage until the Early Tertiary, and during the Paleocene and Eocene thePlatanaceae included forms with elliptical, palmate and pinnate foliage. The history of thePlatanaceae suggests that several features of the reproductive morphology of extant taxa may have arisen in association with a trend toward wind pollination. In the Mid Cretaceous, platanoid foliage partially intergrades with pinnateSapindopsis and pedateDebeya-Dewalquea leaves suggesting a close relationship betweenPlatanaceae andRosidae andFagaceae respectively. TheChloranthaceae, Trochodendrales, andPlatanaceae all occupy a somewhat intermediate position between theMagnoliidae andHamamelidae and are of considerable interest with respect to their role in the initial radiation of nonmagnoliid (higher) dicotyledons.