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.     

The megagametophyte in Anarthria (Anarthriaceae,Poales) and its implications for the phylogeny of the Poales

The development and structure of the megagametophyte of Anarthria (Anarthriaceae), Aphclia, and Centrolepis (Centrolepidaceae) are described. Anarthriaceae has tenuinucellate ovules and the Polygonum type of megagametophyte development, both characters typical of the Poales. However, it lacks the anticlinally elongated nucellar epidermis and numerous large starch bodies observed in the megagametophyte of Centrolepidaceae, both characters also present in Restionaceae. This relatively generalized megagametophyte structure is consistent with data from the chloroplast genome, which suggest that Anarthriaceae are not as closely related to Restionaceae as previously assumed. New data from the megagametophyte are analyzed cladistically together with other available information on the poalean families. The results show that there are two possible positions for Anarthriaceae: either as sister to Poaceae. Joinvilleaceae, Restionaceae, Ecdeiocoleaceae, and Restionaceae, or as sister to only the latter three families. The new data also allow a critical reevaluation of the phylogenetic position of Centrolepidaceae, which is either basal to the poalean clade (based on microgametophyte data), or embedded in the Restionaceae (based on anther structure and megagametophyte data).     

Molecular systematics of Iridaceae: evidence from four plastid DNA regions

Iridaceae are one of the largest families of Lilianae and probably also among the best studied of monocotyledons. To further evaluate generic, tribal, and subfamilial relationships we have produced four plastid DNA data sets for 57 genera of Iridaceae plus outgroups: rps4, rbcL (both protein-coding genes), the trnL intron, and the trnL-F intergenic spacer. All four matrices produce similar although not identical trees, and we thus analyzed them in a combined analysis, which produced a highly resolved and well-supported topology, in spite of the fact that the partition homogeneity test indicated strong incongruence. In each of the individual trees, some genera or groups of genera are misplaced relative to morphological cladistic studies, but the combined analysis produced a pattern much more similar to these previous ideas of relationships. In the combined tree, all subfamilies were resolved as monophyletic, except Nivenioideae that formed a grade in which Ixioideae were embedded. Achlorophyllous Geosiris (sometimes referred to Geosiridaceae or Burmanniaceae) fell within the nivenioid grade. Most of the tribes were monophyletic, and Isophysis (Tasmanian) was sister to the rest of the family; Diplarrhena (Australian) fell in a well-supported position as sister to Irideae/Sisyrinchieae/Tigridieae/Mariceae (i.e., Iridoideae); Bobartia of Sisyrinchieae is supported as a member of Irideae. The paraphyly of Nivenioideae is suspicious due to extremely high levels of sequence divergence, and when they were constrained to be monophyletic the resulting trees were only slightly less parsimonious (<1.0%). However, this subfamily also lacks clear morphological synapomorphies and is highly heterogeneous, so it is difficult to develop a strong case on nonmolecular grounds for their monophyly.     

Ultrastructure of stomatal development in early-divergent angiosperms reveals contrasting patterning and pre-patterning

Background and Aims

Angiosperm stomata consistently possess a pair of guard cells, but differ between taxa in the patterning and developmental origin of neighbour cells. Developmental studies of phylogenetically pivotal taxa are essential as comparative yardsticks for understanding the evolution of stomatal development.

Methods

We present a novel ultrastructural study of developing stomata in leaves of Amborella (Amborellales), Nymphaea and Cabomba (Nymphaeales), and Austrobaileya and Schisandra (Austrobaileyales), representing the three earliest-divergent lineages of extant angiosperms (the ANITA-grade).

Key Results

Alternative developmental pathways occur in early-divergent angiosperms, resulting partly from differences in pre-patterning and partly from the presence or absence of highly polarized (asymmetric) mitoses in the stomatal cell lineage. Amplifying divisions are absent from ANITA-grade taxa, indicating that ostensible similarities with the stomatal patterning of Arabidopsis are superficial. In Amborella, ‘squared’ pre-patterning occurs in intercostal regions, with groups of four protodermal cells typically arranged in a rectangle; most guard-mother cells are formed by asymmetric division of a precursor cell (the mesoperigenous condition) and are typically triangular or trapezoidal. In contrast, water-lily stomata are always perigenous (lacking asymmetric divisions). Austrobaileya has occasional ‘giant’ stomata.

Conclusions

Similar mature stomatal phenotypes can result from contrasting morphogenetic factors, although the results suggest that paracytic stomata are invariably the product of at least one asymmetric division. Loss of asymmetric divisions in stomatal development could be a significant factor in land plant evolution, with implications for the diversity of key structural and physiological pathways.     

Racemose inflorescences of monocots: structural and morphogenetic interaction at the flower/inflorescence level

Background

Understanding and modelling early events of floral meristem patterning and floral development requires consideration of positional information regarding the organs surrounding the floral meristem, such as the flower-subtending bracts (FSBs) and floral prophylls (bracteoles). In common with models of regulation of floral patterning, the simplest models of phyllotaxy consider only unbranched uniaxial systems. Racemose inflorescences and thyrses offer a useful model system for investigating morphogenetic interactions between organs belonging to different axes.

Scope

This review considers (1) racemose inflorescences of early-divergent and lilioid monocots and their possible relationship with other inflorescence types, (2) hypotheses on the morphogenetic significance of phyllomes surrounding developing flowers, (3) patterns of FSB reduction and (4) vascular patterns in the primary inflorescence axis and lateral pedicels.

Conclusions

Racemose (partial) inflorescences represent the plesiomorphic condition in monocots. The presence or absence of a terminal flower or flower-like structure is labile among early-divergent monocots. In some Alismatales, a few-flowered racemose inflorescence can be entirely transformed into a terminal ‘flower’. The presence or absence and position of additional phyllomes on the lateral pedicels represent important taxonomic markers and key features in regulation of flower patterning. Racemose inflorescences with a single floral prophyll are closely related to thyrses. Floral patterning is either unidirectional or simultaneous in species that lack a floral prophyll or possess a single adaxial floral prophyll and usually spiral in the outer perianth whorl in species with a transversely oriented floral prophyll. Inhibitory fields of surrounding phyllomes are relevant but insufficient to explain these patterns; other important factors are meristem space economy and/or the inhibitory activity of the primary inflorescence axis. Two patterns of FSB reduction exist in basal monocots: (1) complete FSB suppression (cryptic flower-subtending bract) and (2) formation of a ‘hybrid’ organ by overlap of the developmental programmes of the FSB and the first abaxial organ formed on the floral pedicel. FSB reduction affects patterns of interaction between the conductive systems of the flower and the primary inflorescence axis.     

The injured lung: clinical issues and experimental models

Exposure of military and civilian populations to inhaled toxic chemicals can take place as a result of deliberate release (warfare, terrorism) or following accidental releases from industrial concerns or transported chemicals. Exposure to inhaled toxic chemicals can result in an acute lung injury, and in severe cases acute respiratory distress syndrome, for which there is currently no specific medical therapy, treatment remaining largely supportive. This treatment often requires intensive care facilities that may become overwhelmed in mass casualty events and may be of limited benefit in severe cases. There remains, therefore, a need for evidence-based treatment to inform both military and civilian medical response teams on the most appropriate treatment for chemically induced lung injury. This article reviews data used to derive potential clinical management strategies for chemically induced lung injury.     

Morphology of Hydatellaceae, an anomalous aquatic family recently recognized as an early-divergent angiosperm lineage

The family Hydatellaceae was recently reassigned to the early-divergent angiosperm order Nymphaeales rather than the monocot order Poales. This dramatic taxonomic adjustment allows comparison with other early-divergent angiosperms, both extant and extinct. Hydatellaceae possess some monocot-like features that could represent adaptations to an aquatic habit. Ecophysiological parallels can also be drawn from fossil taxa that are known from small achene-like diaspores, as in Hydatellaceae. Reproductive units of Hydatellaceae consist of perianthlike bracts enclosing several pistils and/or stamens. In species with bisexual reproductive units, a single unit resembles an "inside-out" flower, in which stamens are surrounded by carpels that are initiated centrifugally. Furthermore, involucre development in Trithuria submersa, with delayed growth of second whorl bracts, resembles similar delayed development of the second perianth whorl in Cabomba. Several hypotheses on the homologies of reproductive units in Hydatellaceae are explored. Currently, the most plausible interpretation is that each reproductive unit represents an aggregation of reduced unisexual apetalous flowers, which are thus very different from flowers of Nymphaeales. Each pistil in Hydatellaceae is morphologically and developmentally consistent with a solitary ascidiate carpel. However, ascidiate carpel development, consistent with placement in Nymphaeales, is closely similar to pseudomonomerous pistil development as in Poaes.     

Comparative ontogeny of the cyathium in Euphorbia (Euphorbiaceae) and its allies: exploring the organ-flower-inflorescence boundary

We present a detailed comparative ontogenetic analysis of pseudanthia of representatives of all three subtribes of Euphorbieae (Euphorbiinae, Neoguillauminiinae, Anthosteminae) in order to clarify their homologies and interpretation. The cyathium of Euphorbia and its allies (subtribe Euphorbiinae) closely resembles a bisexual flower but is traditionally interpreted as an inflorescence bearing clusters of highly reduced male flowers surrounding a single terminal female flower. Previously unreported characters are (1) male flowers formed one above the other in the male inflorescences of some Euphorbiinae, (2) late-developing perianthlike structures in some male flowers of Neoguillauminia cleopatra, (3) evidence for a bracteate origin of the female perianth in Anthosteminae and Neoguillauminiinae, and (4) spatiotemporally independent formation of abscission zone and perianth. Indistinct boundaries between inflorescence, flower, and floral organs demonstrate that defining the cyathium neither as an inflorescence nor as a flower is entirely satisfactory and indicate a "hybrid" flower/inflorescence nature of the cyathium. Based on our current knowledge and the existing phylogenetic context, it is most parsimonious to suggest that the cyathium evolved from a determinate thyrse with a terminal female flower surrounded by dichasial male partial inflorescences. We speculate that the cyathium was formed because of strong condensation and possible overlap between expression zones of regulatory genes.     

Epidermal Patterning and Silica Phytoliths in Grasses: An Evolutionary History

Due to the immense ecological and economic significance of grasses, their highly characteristic long–short epidermal patterning and associated silica phytoliths represent significant diagnostic markers in studies of ancient climate change and agriculture. We explore the link between epidermal cell patterning and phytolith development and review the evolutionary history of phytoliths in the context of recent well-resolved phylogenetic analyses of grasses and allied Poales, focusing on early-divergent grasses and the subfamilies that constitute the BEP group (the bamboos and their allies). Dimorphic epidermal patterning is a common feature of Poaceae and the related family Joinvilleaceae, where phytoliths are located primarily in the short cells. However, Joinvillea lacks the short-cell pairs that occur in many grasses. The costal rows of phytoliths that characterize some grasses could represent loss of long–short cell patterning over the veins. Unlobed phytoliths probably represent the ancestral condition in grasses, though bilobate phytoliths evolved at an early stage. Either transverse-unlobed or transverse-bilobate phytoliths predominate in the early-divergent lineages, whereas axial-bilobates (or polylobates) primarily characterize the PACMAD clade and the BEP subfamily Pooideae.