A comparative study of floral development inTrillium apetalon andT. kamtschaticum (Liliaceae)

Trillium apetalon Makino is unique amongTrillium in having apetalous flowers. Using scanning electron microscope, the early floral development was observed in comparison with that ofT. kamtschaticum Pallas ex Pursh having petalous flowers. Morphologically petal primordia closely resemble stamen primordia in their more or less narrow and radially symmetric shape and are clearly distinct from sepal primordia with broad bases. Early in floral development sepal primordia are first initiated and subsequently two whorls of three primordia each are formed in rapid sequence, the first three at the corners and the second three at the sides of the triangular floral apex. Based on comparison in position and early developmental processes of their primordia, petals and outer stamens ofTrillium kamtschaticum are equivalent to outer stamens and inner stamens ofT. apetalon. The replacement of petals by outer stamens apparently leads to the loss of petals inTrillium apetalon flowers. Such a replacement can be interpreted in terms of homeosis. The replacement of the petal whorl leads to the serial replacement of the subsequent whorls: outer stamens by inner stamens, and inner stamens by gynoecium inTrillium apetalon. The term ‘serial homeosis’ is introduced for this serial replacement.     

Antenna to leg transformation: Dynamics of developmental competence

We explore the transformation of antenna to leg in Drosophila melanogaster, using ectopically expressed transgenes with heat shock promoters: heat shock Antennapedia, heat shock Ultrabithorax, and heat shock mouse Hox A5. We determined the frequency of transformation of several leg markers in response to Antennapedia protein delivered by heat shock at different times and doses. We also studied stage-specific responses to the transgene, heat shock mouse Hox A5. Results show that each marker has its own stage and dose-specific pattern of response. The same marker could pass through a period of high-dose inhibition followed by a dose-independent response and then a positive dose-dependent phase. The heat shock-induced transgenes and spineless aristapedia transformed the apterous enhancer trap antenna disc expression pattern toward the pattern found in leg discs. These results are considered in relation to developmental competence—the ability of developing tissue to respond to internal or external influences. The results suggest that all genes tested interact with the same competence system and that at least two classes of mechanisms are associated with antenna to leg transformation: one comprises global mechanisms that permit transformation over approximately 24 hr; the second class of mechanisms act very locally and are responsible for changes in dose response on the order of 4–8 hr. © 1996 Wiley-Liss, Inc.     

Jaw transformation with gain of symmetry after Dlx5/Dlx6 inactivation: Mirror of the past?

In modern vertebrates upper and lower jaws are morphologically different. Both develop from the mandibular arch, which is colonized mostly by Hox-free neural crest cells. Here we show that simultaneous inactivation of the murine homeobox genes Dlx5 and Dlx6 results in the transformation of the lower jaw into an upper jaw and in symmetry of the snout. This is the first homeotic-like transformation found in this Hox-free region after gene inactivation. A suggestive parallel comes from the paleontological record, which shows that in primitive vertebrates both jaws are essentially mirror images of each other. Our finding supports the notion that Dlx genes are homeotic genes associated with morphological novelty in the vertebrate lineage.     

Flower structure and development of Araceae compared with alismatids and Acoraceae

Floral development of Araceae is compared with that of other basal monocots such as alismatids and Acorus. Flowers of Araceae, Acorus and several alismatids with spicate inflorescences lack a subtending floral bract. In Araceae and some Potamogetonaceae the subtending floral bract is suppressed, and not incorporated into the perianth. This differs from Acorus and some alismatids, where a bract-like median abaxial tepal is formed in the outer perianth whorl (i.e. developmental merger of flower-subtending bract and tepal). In Araceae, Acorus and spicate alismatids flowers develop unidirectionally, correlated with bract reduction. Araceae lack unidirectionality in the outer perianth whorl, in contrast t o Acorus and Juncaginaceae. The transition from trimerous to dimerous flowers in Onintiurn (Araceae) is by accentuation of the unidirectionality of the inner perianth. The gynoecium of Araceae and Acorus is synascidiate. However, in most Araceae the synascidiate portion is shorter than in Acorns, and a distinct basal elongation phase as in Acorus and Juncaginaceae was not found. The perianth and androecium of Lysichiton and Symplocarpus and the gynoecium of Gymnostachys differ from other Araceae and resemble those in Potamogetonaceae. Developmental findings support the isolation of Acorus from Araceae, and show similarities of Araceae with Potamogetonaceae and of Acorus with Juncaginaceae.     

A double-flowered variety of lesser periwinkle (Vinca minor fl. pl.) that has persisted in the wild for more than 160 years

Background and Aims

Homeotic transitions are usually dismissed by population geneticists as credible modes of evolution due to their assumed negative impact on fitness. However, several lines of evidence suggest that such changes in organ identity have played an important role during the origin and subsequent evolution of the angiosperm flower. Better understanding of the performance of wild populations of floral homeotic varieties should help to clarify the evolutionary potential of homeotic mutants. Wild populations of plants with changes in floral symmetry, or with reproductive organs replacing perianth organs or sepals replacing petals have already been documented. However, although double-flowered varieties are quite popular as ornamental and garden plants, they are rarely found in the wild and, if they are, usually occur only as rare mutant individuals, probably because of their low fitness relative to the wild-type. We therefore investigated a double-flowered variety of lesser periwinkle, Vinca minor flore pleno (fl. pl.), that is reported to have existed in the wild for at least 160 years. To assess the merits of this plant as a new model system for investigations on the evolutionary potential of double-flowered varieties we explored the morphological details and distribution of the mutant phenotype.

Methods

The floral morphology of the double-flowered variety and of a nearby population of wild-type plants was investigated by means of visual inspection and light microscopy of flowers, the latter involving dissected or sectioned floral organs.

Key Results

The double-flowered variety was found in several patches covering dozens of square metres in a forest within the city limits of Jena (Germany). It appears to produce fewer flowers than the wild-type, and its flowers are purple rather than blue. Most sepals in the first floral whorl resemble those in the wild-type, although occasionally one sepal is broadened and twisted. The structure of second-whorl petals is very similar to that of the wild-type, but their number per flower is more variable. The double-flowered character is due to partial or complete transformation of stamens in the third whorl into petaloid organs. Occasionally, ‘flowers within flowers’ also develop on elongated pedicels in the double-flowered variety.

Conclusions

The flowers of V. minor fl. pl. show meristic as well as homeotic changes, and occasionally other developmental abnormalities such as mis-shaped sepals or loss of floral determinacy. V. minor fl. pl. thus adds to a growing list of natural floral homeotic varieties that have established persistent populations in the wild. Our case study documents that even mutant varieties that have reproductive organs partially transformed into perianth organs can persist in the wild for centuries. This finding makes it at least conceivable that even double-flowered varieties have the potential to establish new evolutionary lineages, and hence may contribute to macroevolutionary transitions and cladogenesis.     

Floral evolution in the Annonaceae: hypotheses of homeotic mutations and functional convergence

The recent publication of hypotheses explaining the homeotic control of floral organ identity together with the availability of increasingly comprehensive and well‐resolved molecular phylogenies presents an ideal opportunity for reassessing current knowledge of floral diversity and evolution in the Annonaceae. This review summarizes currently available information on selected aspects of floral structure and function, including: changes in the number of perianth whorls and the number of perianth parts per whorl; the evolution of sympetaly; the diversity and evolution of pollination chambers (with a novel classification of seven main structural forms of floral chamber based on the different arrangement, size and shape of petals); the evolution of perianth glands; floral unisexuality and hypotheses explaining the unexpectedly high frequency of occurrence of androdioecy; the origin and possible function of inner and outer staminodes; the evolution of stamen connective diversity and theca septation; and the origin of ‘true’ syncarpy and functionally equivalent extragynoecial compita. In each case, current ideas on the origin, evolution and function are discussed. The information presented in this review enables two main conclusions to be drawn. The first is that changes in the homeotic control of floral organ identity may have had a profound impact on floral structure in several disparate lineages in the family. This is most obvious in Fenerivia, in which a centrifugal shift of floral organ identity has occurred, and in Dasymaschalon, in which a reverse (centripetal) shift has occurred. Other genera that have gained or lost entire perianth whorls are likely to have undergone similar homeotic changes. Attention is also drawn to the extensive functional convergence in Annonaceae flowers, with widespread homoplasy in many characters that have previously been emphasized in higher‐level classifications.     

Roles of synorganisation,zygomorphy and heterotopy in floral evolution: the gynostemium and labellum of orchids and other lilioid monocots

A gynostemium, comprising stamen filaments adnate to a syncarpous style, occurs in only threc groups of monocots: the large family Orchidaceae (Asparagales) and two small genera Pauridia (Hypoxidaceae: Asparagales) and Corsia (Corsiaceae, probably in Liliales), all epigynous taxa. Pauridia has actinomorphic (polysymmetric) flowers, whereas those of Corsia and most orchids are strongly zygomorphic (monosymmetric) with a well-differentiated labellum. In Corsia the labellum is formed from the outer median tepal (sepal), whereas in orchids it is formed from the inner median tepal (petal) and is developmentally adaxial (but positionally abaxial in orchids with resupinate flowers). Furthermore, in orchids zygomorphy is also expressed in the stamen whorls, in contrast to Corsia. In Pauridia a complete stamen whorl is suppressed, but the 'lost' outer whorl is fused to the style. The evolution of adnation and zygomorphy are discussed in the context of the existing phylogenetic framework in monocotyledons. An arguably typological classification of floral terata is presented, focusing on three contrasting modes each of peloria and pseudopeloria. Dynamic evolutionary transitions in floral morphology are assigned to recently revised concepts of heterotopy (including homeosis) and heterochrony, seeking patterns that delimit developmental constraints and allow inferences regarding underlying genetic controls. Current evidence suggests that lateral heterotopy is more frequent than acropetal heterotopy, and that full basipetal heterotopy does not occur. Pseudopeloria is more likely to generate a radically altered yet functional perianth, but is also more likely to cause acropetal modification of the gynostemium. These comparisons indicate that there are at least two key genes or sets of genes controlling adnation, adaxial stamen suppression and labellum development in lilioid monocots; at least one is responsible for stamen adnation to the style (i.e. gynostemium formation), and another controls adaxial stamen suppression and adaxial labellum formation in orchids. Stamen adnation to the style may be a product of over-expression of the genes related to epigyny (i.e. a form of hyper-epigyny). If, as seems likely, stamen-style adnation preceded zygomorphy in orchid evolution, then the flowers of Pauridia may closely resemble those of the immediate ancestors of Orchidaceae, although existing molecular phylogenetic data indicate that a sister-group relationship is unlikely. The initial radiation in Orchidaceae can be attributed to the combination of hyper-epigyny, zygomorphy and resupination, but later radiations at lower taxonomic levels that generated the remarkable species richness of subfamilies Orchidoideae and Epidendroideae are more likely to reflect more subtle innovations that directly influence pollinator specificity, such as the development of stalked pollinaria and heavily marked and/or spur-bearing labella.     

Structure of Flower in Arabidopsis thaliana: Spatial Pattern Formation

Morphological analysis of flowers was carried out in Arabidopsis thaliana wild type plants and agamous and apetala2 mutants. No direct substitution of organs takes place in the mutants, since the number and position of organs in them do not correspond to the structure of wild type flower. In order to explain these data, a notion of spatial pattern formation in the meristem was introduced, which preceded the processes of appearance of organ primordia and formation of organs. Zones of acropetal and basipetal spatial pattern formation in the flower of wild type plants were postulated. It was shown that the acropetal spatial pattern formation alone took place in agamous mutants and basipetal spatial pattern formation alone, in apetala2 mutants. Different variants of flower structure are interpreted as a result of changes in the volume of meristem (space) and order of spatial pattern formation (time).     

Capsella as a model system to study the evolutionary relevance of floral homeotic mutants

Several lines of evidence suggest that homeotic changes played a considerable role during the evolution of flowers. This, however, is difficult to reconcile with the predominant evolutionary theory which rejects any drastic, saltational change of the phenotype as reasonable mode of evolution due to its assumed negative impact on the fitness of the affected organism. A better understanding of the evolutionary potential of homeotic transitions requires a study of the performance of respective mutant varieties in the wild. Here we introduce ``Stamenoid petals' (Spe), a variety of Capsella bursa-pastoris (shepherd's purse), as a suitable model to study the evolutionary potential of floral homeotic mutants. In the flowers of the Spe variety all petals are transformed into stamens, while all other floral organs are unaffected. In contrast to most other homeotic mutants the Spe variety occurs on several locations in relatively large and stable populations in the wild. Due to its close relationship to the model plant Arabidopsis thaliana, the Spe variety of C. bursa-pastoris can be rigorously studied, from the molecular genetic basis of the phenotype to its consequences on the fitness in wild habitats. Investigations on Spe may thus help to clarify whether homeotic transformations have the potential to contribute to macroevolution.