Evolution of unusual morphologies in Lentibulariaceae (bladderworts and allies) and Podostemaceae (river-weeds): a pictorial report at the interface of developmental biology and morphological diversification.

BACKGROUND: Various groups of flowering plants reveal profound ('saltational') changes of their bauplans (architectural rules) as compared with related taxa. These plants are known as morphological misfits that appear as rather large morphological deviations from the norm. Some of them emerged as morphological key innovations (perhaps 'hopeful monsters') that gave rise to new evolutionary lines of organisms, based on (major) genetic changes. SCOPE: This pictorial report places emphasis on released bauplans as typical for bladderworts (Utricularia, approx. 230 secies, Lentibulariaceae) and river-weeds (Podostemaceae, three subfamilies, approx. 54 genera, approx. 310 species). Bladderworts (Utricularia) are carnivorous, possessing sucking traps. They live as submerged aquatics (except for their flowers), as humid terrestrials or as epiphytes. Most Podostemaceae are restricted to rocks in tropical river-rapids and waterfalls. They survive as submerged haptophytes in these extreme habitats during the rainy season, emerging with their flowers afterwards. The recent scientific progress in developmental biology and evolutionary history of both Lentibulariaceae and Podostemaceae is summarized. CONCLUSIONS: Lentibulariaceae and Podostemaceae follow structural rules that are different from but related to those of more typical flowering plants. The roots, stems and leaves - as still distinguishable in related flowering plants - are blurred ('fuzzy'). However, both families have stable floral bauplans. The developmental switches to unusual vegetative morphologies facilitated rather than prevented the evolution of species diversity in both families. The lack of one-to-one correspondence between structural categories and gene expression may have arisen from the re-use of existing genetic resources in novel contexts. Understanding what developmental patterns are followed in Lentibulariaceae and Podostemaceae is a necessary prerequisite to discover the genetic alterations that led to the evolution of these atypical plants. Future molecular genetic work on morphological misfits such as bladderworts and river-weeds will provide insight into developmental and evolutionary aspects of more typical vascular plants.

Fundamentals of Plant Morphology and Plant Evo-Devo (Evolutionary Developmental Morphology).

Morphological concepts are used in plant evo-devo (evolutionary developmental biology) and other disciplines of plant biology, and therefore plant morphology is relevant to all of these disciplines. Many plant biologists still rely on classical morphology, according to which there are only three mutually exclusive organ categories in vascular plants such as flowering plants: root, stem (caulome), and leaf (phyllome). Continuum morphology recognizes a continuum between these organ categories. Instead of Aristotelian identity and either/or logic, it is based on fuzzy logic, according to which membership in a category is a matter of degree. Hence, an organ in flowering plants may be a root, stem, or leaf to some degree. Homology then also becomes a matter of degree. Process morphology supersedes structure/process dualism. Hence, structures do not have processes, they are processes, which means they are process combinations. These process combinations may change during ontogeny and phylogeny. Although classical morphology on the one hand and continuum and process morphology on the other use different kinds of logic, they can be considered complementary and thus together they present a more inclusive picture of the diversity of plant form than any one of the three alone. However, continuum and process morphology are more comprehensive than classical morphology. Insights gained from continuum and process morphology can inspire research in plant morphology and plant evo-devo, especially MorphoEvoDevo.

Phylogeny of the clusioid clade (Malpighiales): evidence from the plastid and mitochondrial genomes.

PREMISE OF THE STUDY: The clusioid clade includes five families (i.e., Bonnetiaceae, Calophyllaceae, Clusiaceae s.s., Hypericaceae, and Podostemaceae) represented by 94 genera and ≈1900 species. Species in this clade form a conspicuous element of tropical forests worldwide and are important in horticulture, timber production, and pharmacology. We conducted a taxon-rich multigene phylogenetic analysis of the clusioids to clarify phylogenetic relationships in this clade. METHODS: We analyzed plastid (matK, ndhF, and rbcL) and mitochondrial (matR) nucleotide sequence data using parsimony, maximum likelihood, and Bayesian inference. Our combined data set included 194 species representing all major clusioid subclades, plus numerous species spanning the taxonomic, morphological, and biogeographic breadth of the clusioid clade. KEY RESULTS: Our results indicate that Tovomita (Clusiaceae s.s.), Harungana and Hypericum (Hypericaceae), and Ledermanniella s.s. and Zeylanidium (Podostemaceae) are not monophyletic. In addition, we place four genera that have not been included in any previous molecular study: Ceratolacis, Diamantina, and Griffithella (Podostemaceae), and Santomasia (Hypericaceae). Finally, our results indicate that Lianthus, Santomasia, Thornea, and Triadenum can be safely merged into Hypericum (Hypericaceae). CONCLUSIONS: We present the first well-resolved, taxon-rich phylogeny of the clusioid clade. Taxon sampling and resolution within the clade are greatly improved compared to previous studies and provide a strong basis for improving the classification of the group. In addition, our phylogeny will form the foundation for our future work investigating the biogeography of tropical angiosperms that exhibit Gondwanan distributions.

A Historical Perspective of Bladderworts (Utricularia): Traps, Carnivory and Body Architecture.

The genus Utricularia includes around 250 species of carnivorous plants, commonly known as bladderworts. The generic name Utricularia was coined by Carolus Linnaeus in reference to the carnivorous organs (Utriculus in Latin) present in all species of the genus. Since the formal proposition by Linnaeus, many species of Utricularia were described, but only scarce information about the biology for most species is known. All Utricularia species are herbs with vegetative organs that do not follow traditional models of morphological classification. Since the formal description of Utricularia in the 18th century, the trap function has intrigued naturalists. Historically, the traps were regarded as floating organs, a common hypothesis that was maintained by different botanists. However, Charles Darwin was most likely the first naturalist to refute this idea, since even with the removal of all traps, the plants continued to float. More recently, due mainly to methodological advances, detailed studies on the trap function and mechanisms could be investigated. This review shows a historical perspective on Utricularia studies which focuses on the traps and body organization.

Evo-devo and the search for homology ("sameness") in biological systems.

Developmental biology and evolutionary studies have merged into evolutionary developmental biology ("evo-devo"). This synthesis already influenced and still continues to change the conceptual framework of structural biology. One of the cornerstones of structural biology is the concept of homology. But the search for homology ("sameness") of biological structures depends on our favourite perspectives (axioms, paradigms). Five levels of homology ("sameness") can be identified in the literature, although they overlap to some degree: (i) serial homology (homonomy) within modular organisms, (ii) historical homology (synapomorphy), which is taken as the only acceptable homology by many biologists, (iii) underlying homology (i.e., parallelism) in closely related taxa, (iv) deep evolutionary homology due to the "same" master genes in distantly related phyla, and (v) molecular homology exclusively at gene level. The following essay gives emphasis on the heuristic advantages of seemingly opposing perspectives in structural biology, with examples mainly from comparative plant morphology. The organization of the plant body in the majority of angiosperms led to the recognition of the classical root-shoot model. In some lineages bauplan rules were transcended during evolution and development. This resulted in morphological misfits such as the Podostemaceae, peculiar eudicots adapted to submerged river rocks. Their transformed "roots" and "shoots" fit only to a limited degree into the classical model which is based on either-or thinking. It has to be widened into a continuum model by taking over elements of fuzzy logic and fractal geometry to accommodate for lineages such as the Podostemaceae.

Sympodial construction of Fibonacci-type leaf rosettes in Pinguicula moranensis (Lentibulariaceae).

BACKGROUND AND AIMS: The leaf rosettes of the carnivorous Pinguicula moranensis follow a spiral phyllotaxis approaching a Fibonacci pattern while the stalked flowers arise from extra-axillary sites between the leaves. The organization of this rosette has been discussed by various authors, with various results. The aim of the present study was to clarify the development of the flowering rosettes of this species. METHODS: The formation of the rosettes is shown with the aid of scanning electron microscopy. KEY RESULTS AND CONCLUSIONS: The scanning electron micrographs show that each flower terminates an article (sympodial unit). The leaves of consecutive articles of such sympodially constructed rosettes are arranged along a spiral Fibonacci pattern (with divergence angles around 137 degrees). This results from homodromy of leaf initiation in consecutive articles with the first leaf (prophyll) of a new article inserted in an obliquely transverse position next to the floral scape that terminates the former article. Sympodial construction of flowering shoots and leaf rosettes is also known from Aloe, Gunnera and Philodendron. As a by-product of this study, the unidirectional development of the Pinguicula flower is confirmed and discussed.

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.

Morphology and development of the female flowers in Geonoma interrupta (Arecaceae).

Morphology and development of the female flowers in Geonoma interrupta are described and compared with other taxa within Arecaceae. Inflorescences are pleiothyrses. Cincinni are immersed in pits and arranged according to the Fibonacci pattern along the rachillae. The gynoecium is composed of three free carpels in early stages and later becomes pseudomonomerous. Two carpels are sterile; they develop to different degrees and are commonly unequal in size. The fertile carpel contains a single, crassinucellate, anatropous ovule. Styles are formed in each carpel. The style of the fertile carpel becomes basifixed as the ovary enlarges. The stigmas remain free and plicate during development and expose unicellular papillae at anthesis. Pollen tube transmitting tracts and a compitum are present in the ventral slits of the stigmas and the postgenitally united styles during anthesis. A septal nectary is formed by incomplete union of the flanks of the carpels at the base of the gynoecium, and nectar is secreted from an epithelium. It is suggested that in Geonoma as a whole, the attraction of pollinators to female flowers is due to a combination of nectar reward and partial mimicry of male flowers.