Floral variation and floral genetics in basal angiosperms

Recent advances in phylogeny reconstruction and floral genetics set the stage for new investigations of the origin and diversification of the flower. We review the current state of angiosperm phylogeny, with an emphasis on basal lineages. With the surprising inclusion of Hydatellaceae with Nymphaeales, recent studies support the topology of Amborella sister to all other extant angiosperms, with Nymphaeales and then Austrobaileyales as subsequent sisters to all remaining angiosperms. Notable modifications from most recent analyses are the sister relationships of Chloranthaceae with the magnoliids and of Ceratophyllaceae with eudicots. We review "trends" in floral morphology and contrast historical, intuitive interpretations with explicit character-state reconstructions using molecular-based trees, focusing on (1) the size, number, and organization of floral organs; (2) the evolution of the perianth; (3) floral symmetry; and (4) floral synorganization. We provide summaries of those genes known to affect floral features that contribute to much of floral diversity. Although most floral genes have not been investigated outside of a few model systems, sufficient information is emerging to identify candidate genes for testing specific hypotheses in nonmodel plants. We conclude with a set of evo-devo case studies in which floral genetics have been linked to variation in floral morphology.     

Floral structure and development of Acoraceae and its systematic relationships with basal angiosperms

Flower development and anatomy of Acorus calamus and flower anatomy of A. gramineus were studied. Findings were compared with published reports on paleoherbs. Important developmental features include an abaxially median tepal that is initiated first and is similar to a flower-subtending bract and unidirectional flower development with an inversion of organ initiation sequence in the second tepal whorl. The mature gynoecium is largely synascidiate, but early development of carpels is plicate, and the apocarpous portion persists up to anthesis. The carpels form dorsal bulges on the style, enclosing longitudinal intercarpellary slits. The dominance of the synascidiate portion and the apical position of the placenta result from a late and distinct basal elongation of the gynoecium. Stigma, pollen transmitting tract, and ovary are filled with secretion. Secretory papillae are present from the stigma to the placenta; papillae also occur on the rims of the integuments of the ovules. In the uppermost part of the inflorescence, the adaxial floral sectors are reduced in number and structure, and at the apex of the inflorescence, a peloria-like structure is formed. Developmental and morphological similarities seem to be closer between Acorus and Piperales than between Acorus and other magnoliids.     

Stomatal architecture and evolution in basal angiosperms

Stomatal architecture-the number, form, and arrangement of specialized epidermal cells associated with stomatal guard cells-of 46 species of basal angiosperms representing all ANITA grade families and Chloranthaceae was investigated. Leaf clearings and cuticular preparations were examined with light microscopy, and a sample of 100 stomata from each specimen was coded for stomatal type and five other characters contributing to stomatal architecture. New stomatal types were defined, and many species were examined and illustrated for the first time. Character evolution was examined in light of the ANITA hypothesis using MacClade software. Analysis of character evolution, along with other evidence from this study and evidence from the literature on fossil angiosperms and other seed plant lineages, suggests that the ancestral condition of angiosperms can be described as anomo-stephanocytic, a system in which complexes lacking subdidiaries (anomocytic) intergrade with those having weakly differentiated subsidiaries arranged in a rosette (stephanocytic). From this ancestral condition, tangential divisions of contact cells led to the profusion of different types seen in early fossil angiosperms and Amborellaceae, Austrobaileyales, and derived Chloranthaceae, while the state in Nymphaeales is little modified. Formation of new, derived types by tangential division appears to be a recurrent theme in seed plant evolution.     

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.     

Floral development and floral phyllotaxis in Anaxagorea (Annonaceae)

Background and Aims Anaxagorea is the phylogenetically basalmost genus in the large tropical Annonaceae (custard apple family) of Magnoliales, but its floral structure is unknown in many respects. The aim of this study is to analyse evolutionarily interesting floral features in comparison with other genera of the Annonaceae and the sister family Eupomatiaceae. Methods Live flowers of Anaxagorea crassipetala were examined in the field with vital staining, liquid-fixed material was studied with scanning electron microscopy, and microtome section series were studied with light microscopy. In addition, herbarium material of two other Anaxagorea species was cursorily studied with the dissecting microscope. Key Results Floral phyllotaxis in Anaxagorea is regularly whorled (with complex whorls) as in all other Annonaceae with a low or medium number of floral organs studied so far (in those with numerous stamens and carpels, phyllotaxis becoming irregular in the androecium and gynoecium). The carpels are completely plicate as in almost all other Annonaceae. In these features Anaxagorea differs sharply from the sister family Eupomatiaceae, which has spiral floral phyllotaxis and ascidiate carpels. Flat stamens and the presence of inner staminodes differ from most other Annonaceae and may be plesiomorphic in Anaxagorea. However, the inner staminodes appear to be non-secretory in most Anaxagorea species, which differs from inner staminodes in other families of Magnoliales (Eupomatiaceae, Degeneriacae, Himantandraceae), which are secretory. Conclusions Floral phyllotaxis in Anaxagorea shows that there is no signature of a basal spiral pattern in Annonaceae and that complex whorls are an apomorphy not just for a part of the family but for the family in its entirety, and irregular phyllotaxis is derived. This and the presence of completely plicate carpels in Anaxagorea makes the family homogeneous and distinguishes it from the closest relatives in Magnoliales.     

The evolution of floral biology in basal angiosperms

In basal angiosperms (including ANITA grade, magnoliids, Choranthaceae, Ceratophyllaceae) almost all bisexual flowers are dichogamous (with male and female functions more or less separated in time), and nearly 100 per cent of those are protogynous (with female function before male function). Movements of floral parts and differential early abscission of stamens in the male phase are variously associated with protogyny. Evolution of synchronous dichogamy based on the day/night rhythm and anthesis lasting 2 days is common. In a few clades in Magnoliales and Laurales heterodichogamy has also evolved. Beetles, flies and thrips are the major pollinators, with various degrees of specialization up to large beetles and special flies in some large-flowered Nymphaeaceae, Magnoliaceae, Annonaceae and Aristolochiaceae. Unusual structural specializations are involved in floral biological adaptations (calyptras, inner staminodes, synandria and food bodies, and secretory structures on tepals, stamens and staminodes). Numerous specializations that are common in monocots and eudicots are absent in basal angiosperms. Several families are poorly known in their floral biology.     

Floral symmetry affects speciation rates in angiosperms

Despite much recent activity in the field of pollination biology, the extent to which animal pollinators drive the formation of new angiosperm species remains unresolved. One problem has been identifying floral adaptations that promote reproductive isolation. The evolution of a bilaterally symmetrical corolla restricts the direction of approach and movement of pollinators on and between flowers. Restricting pollinators to approaching a flower from a single direction facilitates specific placement of pollen on the pollinator. When coupled with pollinator constancy, precise pollen placement can increase the probability that pollen grains reach a compatible stigma. This has the potential to generate reproductive isolation between species, because mutations that cause changes in the placement of pollen on the pollinator may decrease gene flow between incipient species. I predict that animal-pollinated lineages that possess bilaterally symmetrical flowers should have higher speciation rates than lineages possessing radially symmetrical flowers. Using sister-group comparisons I demonstrate that bilaterally symmetric lineages tend to be more species rich than their radially symmetrical sister lineages. This study supports an important role for pollinator-mediated speciation and demonstrates that floral morphology plays a key role in angiosperm speciation.     

Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators

The ABC model of floral organ identity is based on studies of Arabidopsis and Antirrhinum, both of which are highly derived eudicots. Most of the genes required for the ABC functions in Arabidopsis and Antirrhinum are members of the MADS-box gene family, and their orthologs are present in all major angiosperm lineages. Although the eudicots comprise 75% of all angiosperms, most of the diversity in arrangement and number of floral parts is actually found among basal angiosperm lineages, for which little is known about the genes that control floral development. To investigate the conservation and divergence of expression patterns of floral MADS-box genes in basal angiosperms relative to eudicot model systems, we isolated several floral MADS-box genes and examined their expression patterns in representative species, including Amborella (Amborellaceae), Nuphar (Nymphaeaceae) and Illicium (Austrobaileyales), the successive sister groups to all other extant angiosperms, plus Magnolia and Asimina, members of the large magnoliid clade. Our results from multiple methods (relative-quantitative RT-PCR, real-time PCR and RNA in situ hybridization) revealed that expression patterns of floral MADS-box genes in basal angiosperms are broader than those of their counterparts in eudicots and monocots. In particular, (i) AP1 homologs are generally expressed in all floral organs and leaves, (ii) AP3/PI homologs are generally expressed in all floral organs and (iii) AG homologs are expressed in stamens and carpels of most basal angiosperms, in agreement with the expectations of the ABC model; however, an AG homolog is also expressed in the tepals of Illicium. The broader range of strong expression of AP3/PI homologs is inferred to be the ancestral pattern for all angiosperms and is also consistent with the gradual morphological intergradations often observed between adjacent floral organs in basal angiosperms.     

Comparative embryology of basal angiosperms

Recent phylogenetic analyses of basal angiosperms have identified those lineages central to the study of the origin and early diversification of flowering plants. As we begin to understand the early evolution of endosperm developmental patterns in flowering plants, it is apparent that we know little about the other basic embryological features of basal angiosperms, such as the nature of the female gametophyte and even whether a process of double fertilization occurs.     

Molecular evolution and phylogenetic utility of the petD group II intron: a case study in basal angiosperms

Sequences of spacers and group I introns in plant chloroplast genomes have recently been shown to be very effective in phylogenetic reconstruction at higher taxonomic levels and not only for inferring relationships among species. Group II introns, being more frequent in those genomes than group I introns, may be further promising markers. Because group II introns are structurally constrained, we assumed that sequences of a group II intron should be alignable across seed plants. We designed universal amplification primers for the petD intron and sequenced this intron in a representative selection of 47 angiosperms and three gymnosperms. Our sampling of taxa is the most representative of major seed plant lineages to date for group II introns. Through differential analysis of structural partitions, we studied patterns of molecular evolution and their contribution to phylogenetic signal. Nonpairing stretches (loops, bulges, and interhelical nucleotides) were considerably more variable in both substitutions and indels than in helical elements. Differences among the domains are basically a function of their structural composition. After the exclusion of four mutational hotspots accounting for less than 18% of sequence length, which are located in loops of domains I and IV, all sequences could be aligned unambiguously across seed plants. Microstructural changes predominantly occurred in loop regions and are mostly simple sequence repeats. An indel matrix comprising 241 characters revealed microstructural changes to be of lower homoplasy than are substitutions. In showing Amborella first branching and providing support for a magnoliid clade through a synapomorphic indel, the petD data set proved effective in testing between alternative hypotheses on the basal nodes of the angiosperm tree. Within angiosperms, group II introns offer phylogenetic signal that is intermediate in information content between that of spacers and group I introns on the one hand and coding sequences on the other.     

The evolution of apomixis in angiosperms: A reappraisal

Abstract

Apomixis, the asexual reproduction via seed, has long been regarded a blind alley of evolution. This hypothesis was based on the assumption that apomixis is an irreversible, phylogenetically derived trait that would rapidly lead to extinction of the respective lineages. However, recent updates of the taxonomic distribution of apomixis in angiosperms suggest an alternative evolutionary scenario. Apomixis is taxonomically scattered and occurs in both early and late branching lineages, with several reversals from apomixis to obligate sex along phylogeny. Genetic control of apomixis is based on altered expression patterns of the same genes that control sexual development; epigenetic changes following polyploidization and/or hybridization may trigger shifts from sexuality to apomixis. Mendelian inheritance confirms the facultative nature and possible reversibility of apomixis to sexual reproduction. Apomixis, therefore, could represent a transition period in the evolution of polyploid complexes, with polyspory in paleopolyploids being a remnant of lost apomixis. In neopolyploids, apomixis helps to overcome sterility and allows for geographical range expansions of agamic polyploid complexes. The facultative nature of apomixis allows for reversal to sexuality and further speciation of paleopolyploid lineages. Thus, apomixis may facilitate diversification of polyploid complexes and evolution in angiosperms.     

Floral morphology and evolution in Anisophylleaceae

TOBE, H. & RAVEN, P. H., 1988. Floral morphology and evolution in Anisophylleaceae. The four genera of Anisophylleaceae ( Anisophyllea, Combretocarpus, Poga , and Polygonanthus ) are very uniform in their floral structures. Characteristic floral features of the family are: flowers small (except for the female flowers of Polygonanthus ), merism nearly fixed (i.e. 3- or 4-mery), petals deeply incised (except in Polygonanthus ), ovary inferior and multi-loculed, ovules few (one or two) per carpel, styles separate, intra- and interstaminal nectariferous tissues present, and floral vasculature simple. Comparisons with related groups support the distinctiveness of Anisophylleaceae, and suggest a close affinity with both Rhizophoraceae and the Myrtales. The presence of incised petals in both groups suggests an especially close relationship between Anisophylleaceae and Rhizophoraceae, while new evidence from comparative floral morphology suggests that Anisophylleaceae occupy an intermediate position between Rhizophoraceae and Myrtales. Within the Anisophylleaceae, Poga and Polygonanthus share several synapomorphies in floral structure, while Combretocarpus is the most divergent genus in the family and is more distantly related to Poga and Polygonanthus . It is uncertain whether Anisophyllea is more closely related to Poga and Polygonanthus or Combretocarpus , because the evidence from comparative floral morphology conflicts with that from embryology; more data from other kinds of characters are needed to resolve this issue.     

Gynoecium evolution in angiosperms: Monomery,pseudomonomery, and mixomery

The presence of a gynoecium composed of carpels is a key feature of angiosperms. The carpel is often regarded as a homologue of the gymnosperm megasporophyll (that is, an ovule-bearing leaf), but higher complexity of the morphological nature of carpel cannot be ruled out. Angiosperm carpels can fuse to form a syncarpous gynoecium. A syncarpous gynoecium usually includes a well-developed compitum, an area where the pollen tube transmitting tracts of individual carpels unite to enable the transition of pollen tubes from one carpel to another. This phenomenon is a precondition to the emergence of carpel dimorphism manifested as the absence of a functional stigma or fertile ovules in part of the carpels. Pseudomonomery, which is characterized by the presence of a fertile ovule (or ovules) in one carpel only, is a specific case of carpel dimorphism. A pseudomonomerous gynoecium usually has a single plane of symmetry and is likely to share certain features of the regulation of morphogenesis with the monosymmetric perianth and androecium. A genuine monomerous gynoecium consists of a single carpel. Syncarpous gynoecia can be abruptly transformed into monomerous gynoecia in the course of evolution or undergo sterilization and gradual reduction of some carpels. Partial or nearly complete loss of carpel individuality that precludes the assignment of an ovule (or ovules) to an individual carpel is observed in a specific group of gynoecia. We termed this phenomenon mixomery, since it should be distinguished from pseudomonomery.     

The ABC model and its applicability to basal angiosperms

BACKGROUND: Although the flower is the central feature of the angiosperms, little is known of its origin and subsequent diversification. The ABC model has long been the unifying paradigm for floral developmental genetics, but it is based on phylogenetically derived eudicot models. Synergistic research involving phylogenetics, classical developmental studies, genomics and developmental genetics has afforded valuable new insights into floral evolution in general, and the early flower in particular. SCOPE AND CONCLUSIONS: Genomic studies indicate that basal angiosperms, and by inference the earliest angiosperms, had a rich tool kit of floral genes. Homologues of the ABCE floral organ identity genes are also present in basal angiosperm lineages; however, C-, E- and particularly B-function genes are more broadly expressed in basal lineages. There is no single model of floral organ identity that applies to all angiosperms; there are multiple models that apply depending on the phylogenetic position and floral structure of the group in question. The classic ABC (or ABCE) model may work well for most eudicots. However, modifications are needed for basal eudicots and, the focus of this paper, basal angiosperms. We offer 'fading borders' as a testable hypothesis for the basal-most angiosperms and, by inference, perhaps some of the earliest (now extinct) angiosperms.     

Flavonoids and the evolution of the angiosperms

Data on the distribution of flavonoids in the angiosperms are summarized and patterns of occurence are shown to be related to plant evolution. Different flavonoid types are regarded as primitive or advanced characters on the basis of biosynthetic complexity and on correlated frequencies of occurrence with morphological and anatomical features. The evolutionary significance of distribution patterns of proanthocyanidins, glycosylflavones, biflavonoids, 6- and 8-hydroxyflavonoids and anthocyanins is discussed in turn. The importance of these various distribution patterns is considered in relation to an ecological function for these flavonoids.     

Primate origins and the evolution of angiosperms

Traditionally, the morphological traits of primates were assumed to be adaptations to an arboreal way of life. However, Cartmill [1972] pointed out that a number of morphological traits characteristic of primates are not found in many other arboreal mammals. He contends that orbital convergence and grasping extremities indicate that the initial divergence of primates involved visual predation on insects in the lower canopy and undergrowth of the tropical forest. However, recent research on nocturnal primates does not support the visually-oriented predation theory. Although insects were most likely important components of the diets of the earliest euprimates, it is argued here that visual predation was not the major impetus for the evolution of the adaptive traits of primates. Recent paleobotanical research has yielded evidence that a major evolutionary event occurred during the Eocene, involving the angiosperms and their dispersal agents. As a result of long-term diffuse coevolutionary interactions with flowering plants, modern primates, bats, and plant-feeding birds all first arose around the Paleocene-Eocene boundary and became the major seed dispersers of modern tropical flora during the Eocene. Thus, it is suggested here that the multitude of resources available on the terminal branches of the newly evolved angiosperm, rain forest trees led to the morphological adaptations of primates of modern aspect.     

Floral development in the androdioecious tree Tapiscia sinensis: Implications for the evolution to androdioecy

The evolutionary pathway between hermaphroditism and dioecy (females and males in a single population) draws widespread interests, and androdioecy (bisexuals and males in a single population) is rarely achieved as an intermediate state between the two breeding systems. Flower bud differentiations in the pistils of hermaphrodites and the pistillodes of males in androdioecious Tapiscia sinensis Oliv. are investigated by routine paraffin section technology, light microscopy, and scanning electron microscopy. A phylogenetic approach is used to analyze the origin of androdioecy. In T. sinensis, hermaphroditic flowers (HF) and male flowers (MF) experienced a similar development pattern in early flower bud differentiation, including the initiation of tepals and stamens. However, the carpel differentiation of MF and HF proceed in different patterns. In HF, the central zone bulges out and produces a ring meristem on which two to three carpel primordia emerge, which eventually developed into a normal pistil with a stigma, a style, and an ovary. However, in most MF, vestigial pistils are stem‐like (type I), and very few have an empty ovary (type II) or a sterile ovule (type III). Moreover, the evolution of sexual systems within the Huerteales indicates that hermaphroditism is the primitive character of T. sinensis. Tapiscia sinensis shows different degrees of reduction between male flowers and bisexual ones in the evolution to dioecy. Functional androdioecy originated from a hermaphroditic ancestor in T. sinensis and, as an intermediate sexual system, involves evolution from hermaphrodites to dioecy.     

Floral structure and evolution in the Anacardiaceae

WANNAN, B. S. & QUINN, C. J, 1991. Floral structure and evolution in the Anacardiaceae. Carpel morphology and anatomy is investigated in 17 genera and carpellode morphology in 12 genera. There is an evolutionary sequence in the family from poorly differentiated, nearly apocarpous gynoecia towards syncarpous gynoecia with clearly defined stigmata, styles and ovaries. There has also been marked reduction culminating in pseudomonomery. The carpellodes of the male flowers appear more conservative, and provide evidence of affinities between genera with quite different fertile gynoecia. The characters have been polarized using Burseraceae as a sister group. Data from these sources, as well as from pericarp anatomy, wood anatomy and biflavonoid content indicate that the long standing intrafamilial classification into five tribes is artificial, and that the two small satellite families, Blepharocaryaceae and Julianiaceae should be included in the family. A large monophyletic group is recognized comprised of essentially four of the existing tribes (Anacardiëae, Dobineëae, Semecarpeae, Rhoëae), as well as the two satellite families. This group incorporates two subgroups of more closely allied genera. The remaining genera (mostly Spondiadeae) are very diverse, and for the present are placed in an artificial group characterised by a set of plesiomorphs. Relationships within this group must be resolved before a satisfactory taxonomy of the family can be achieved.