Unique floral structures and iterative evolutionary themes in Asparagales: Insights from a morphological cladistic analysis

A morphological cladistic analysis is presented of the lilioid order Asparagales, with emphasis on relationships within the “lower” asparagoids, in the context of recent new data on both floral and vegetative structures. The analysis retrieved a monophyletic “lower” asparagoid clade, in contrast to molecular analyses, in which lower asparagoids invariably form a grade. However, limited outgroup sampling in the current analysis is a significant factor in this “inside-out” topology; if the morphological tree is rerooted with Orchidaceae as the outgroup, the result is a topology broadly similar to the molecular one. The relatively low resolution of the “lower” asparagoid clade identified here is a result of high homoplasy in several characters, which could be regarded as iterative evolutionary themes within Asparagales, notably (among floral characters) epigyny and zygomorphy. Close relationships between some family pairs were inferred, including Orchidaceae and Hypoxidaceae, Boryaceae and Blandfordiaceae, Asphodelaceae and Hemerocallidaceae, and Iridaceae and Doryanthaceae. The small South African genusPauridia, which differs from other Hypoxidaceae in that it lacks the outer stamen whorl, was placed as sister to Orchidaceae rather than being embedded in Hypoxidaceae as in molecular analyses, because despite some significant similarities with other Hypoxidaceae (e.g., mucilage canals), it shares some characters with Orchidaceae, notably the presence of a gynostemium and pontoperculate pollen.Xanthorrhoea andLanaria were wild-card taxa in the context of this analysis, with characters in common with more than one different group.     

Evolutionary change in flowers and inflorescences: evidence from naturally occurring terata

Records of naturally occurring, heritable floral abnormalities considerably enhance our understanding of floral evolution. Peloric mutants, frequent in natural populations of orchids and mints, have radially symmetric flowers but occur in species characterized by bilaterally symmetric flowers. Three distributions of peloric flowers across an inflorescence are: (1) complete (all flowers peloric, as in the cycloidea mutant of Antirrhinum), (2) scattered (with both peloric and zygomorphic flowers, as in the epigenetic cycloidea mutant of Linaria), and (3) terminal (only the terminal flower peloric, as in the centroradialis mutant of Antirrhinum). Genetic relationships between lateral and terminal peloria, and between peloric and pseudopeloric flowers, remain ambiguous. Complete peloria probably caused occasional evolutionary reversals from zygomorphy to actinomorphy, whereas the 'terminal-flower effect' is a less likely cause of floral evolution.     

Leaf surface development and the plant fossil record: stomatal patterning in Bennettitales

Stomata play a critical ecological role as an interface between the plant and its environment. Although the guard‐cell pair is highly conserved in land plants, the development and patterning of surrounding epidermal cells follow predictable pathways in different taxa that are increasingly well understood following recent advances in the developmental genetics of the plant epidermis in model taxa. Similarly, other aspects of leaf development and evolution are benefiting from a molecular–genetic approach. Applying this understanding to extinct taxa known only from fossils requires use of extensive comparative morphological data to infer ‘fossil fingerprints’ of developmental evolution (a ‘palaeo‐evo‐devo’ perspective). The seed‐plant order Bennettitales, which flourished through the Mesozoic but became extinct in the Late Cretaceous, displayed a consistent and highly unusual combination of epidermal traits, despite their diverse leaf morphology. Based on morphological evidence (including possession of flower‐like structures), bennettites are widely inferred to be closely related to angiosperms and hence inform our understanding of early angiosperm evolution. Fossil bennettites – even purely vegetative material – can be readily identified by a combination of epidermal features, including distinctive cuticular guard‐cell thickenings, lobed abaxial epidermal cells (‘puzzle cells’), transverse orientation of stomata perpendicular to the leaf axis, and a pair of lateral subsidiary cells adjacent to each guard‐cell pair (termed paracytic stomata). Here, we review these traits and compare them with analogous features in living taxa, aiming to identify homologous – and hence phylogenetically informative – character states and to increase understanding of developmental mechanisms in land plants. We propose a range of models addressing different aspects of the bennettite epidermis. The lobed abaxial epidermal cells indicate adaxial–abaxial leaf polarity and associated differentiated mesophyll that could have optimised photosynthesis. The typical transverse orientation of the stomata probably resulted from leaf expansion similar to that of a broad‐leaved monocot such as Lapageria, but radically different from that of broad‐leafed eudicots such as Arabidopsis. Finally, the developmental origin of the paired lateral subsidiary cells – whether they are mesogene cells derived from the same cell lineage as the guard‐mother cell, as in some eudicots, or perigene cells derived from an adjacent cell lineage, as in grasses – represents an unusually lineage‐specific and well‐characterised developmental trait. We identify a close similarity between the paracytic stomata of Bennettitales and the ‘living fossil’ Gnetum, strongly indicating that (as in Gnetum) the pair of lateral subsidiary cells of bennettites are both mesogene cells. Together, these features allow us to infer development in this diverse and relatively derived lineage that co‐existed with the earliest recognisable angiosperms, and suggest that the use of these characters in phylogeny reconstruction requires revision.     

Systematic root anatomy of Asparagales and other monocotyledons

Root anatomy of several taxa of Asparagales and some taxa formerly included in Asparagales is described in a systematic context together with a literature review. The presence of a dimorphic outer layer with long and short cells is widespread in monocotyledons, indicating that it originated early in the monocot lineage, but whereas this layer is rhizodermal in most monocotyledons, in Asparagales and Araceae it is usually hypodermal. There may be a correlation between the presence of a velamen or a persistent rhizodermis in many Asparagales and Araceae and the presence of a dimorphic hypodermal layer. Many other root anatomical characters, such as the presence of vascular bundles in the central pith and a multi-layered sclerenchymatous cylinder, are probably xeromorphic and developed convergently.     

Cabomba as a model for studies of early angiosperm evolution

BACKGROUND: The angiosperms, or flowering plants, diversified in the Cretaceous to dominate almost all terrestrial environments. Molecular phylogenetic studies indicate that the orders Amborellales, Nymphaeales and Austrobaileyales, collectively termed the ANA grade, diverged as separate lineages from a remaining angiosperm clade at a very early stage in flowering plant evolution. By comparing these early diverging lineages, it is possible to infer the possible morphology and ecology of the last common ancestor of the extant angiosperms, and this analysis can now be extended to try to deduce the developmental mechanisms that were present in early flowering plants. However, not all species in the ANA grade form convenient molecular-genetic models. SCOPE: The present study reviews the genus Cabomba (Nymphaeales), which shows a range of features that make it potentially useful as a genetic model. We focus on characters that have probably been conserved since the last common ancestor of the extant flowering plants. To facilitate the use of Cabomba as a molecular model, we describe methods for its cultivation to flowering in the laboratory, a novel Cabomba flower expressed sequence tag database, a well-adapted in situ hybridization protocol and a measurement of the nuclear genome size of C. caroliniana. We discuss the features required for species to become tractable models, and discuss the relative merits of Cabomba and other ANA-grade angiosperms in molecular-genetic studies aimed at understanding the origin of the flowering plants.     

Systematics and biology of silica bodies in monocotyledons

Many plants take up soluble monosilicic acid from the soil. Some of these plants subsequently deposit it as cell inclusions of characteristic structure. This article describes the distribution and diversity of opaline silica bodies in monocotyledons in a phylogenetic framework, together with a review of techniques used for their examination, and the ecology, function and economic applications of these cell inclusions. There are several different morphological forms of silica in monocot tissues, and the number of silica bodies per cell may also vary. The most common type is the “druse-like” spherical body, of which there is normally a single body per cell, more in some cases. Other forms include the conical type and an amorphous, fragmentary type (silica sand). Silica bodies are most commonly found either in the epidermis (e.g., in grasses, commelinas and sedges) or in the sheath cells of vascular bundles (e.g., in palms, bananas and orchids). Silica-bearing cells are most commonly associated either with subepidermal sclerenchyma or bundle-sheath sclerenchyma. Silica bodies are found only in orchids and commelinids, not in other lilioid or basal monocots. In orchids, silica bodies are entirely absent from subfamilies Vanilloideae and Orchidoideae and most Epidendroideae but present in some Cypripedioideae and in the putatively basal orchid subfamily Apostasioideae. Among commelinid monocots, silica bodies are present in all palms, Dasypogonaceae and Zingiberales but present or absent in different taxa of Poales and Commelinales, with at least four separate losses of silica bodies in Poales.     

Leaf anatomy and relationships of Dietes (Iridaceae)

The leaf anatomy of Dietes is described, including all 6 species. Characters support the morphological evidence that Dietes is a distinct genus and related to other Iridoideae. Certain features, notably the epidermal structure and sheath vasculature, distinguish it from other Iridaceous genera, although the sheath vasculature indicates a relationship with some New World Iridoideae. The leaf margin type is similar to that of other Old World Iridoideae. Many leaf anatomical characters in Dietes are associated with xeromorphy. Leaf anatomy supports the division of Dietes into 2 subgenera.     

Floral anatomy of Bromeliaceae, with particular reference to the evolution of epigyny and septal nectaries in commelinid monocots

Floral anatomy is described in ten genera of Bromeliaceae, including three members of subfamily Bromelioideae, three Tillandsioideae, and four genera of the polyphyletic subfamily Pitcairnioideae (including Brocchinia, the putatively basal genus of Bromeliaceae). Bromeliaceae are probably unique in the order Poales in possessing septal nectaries and epigynous or semi-epigynous flowers. Evidence presented here from floral ontogeny, vasculature, and the relative positions of nectary and ovules indicates that there could have been one or more reversals to apparent hypogyny in Bromeliaceae, although this hypothesis requires a better-resolved phylogeny. Such evolutionary reversals probably evolved in response to specialist pollinators, and in conjunction with other aspects of floral morphology of Bromeliaceae, such as the petal appendages of some species. The ovary is initiated in an inferior position even in semi-epigynous or hypogynous species. The ovary of all so-called hypogynous Bromeliaceae is actually semi-inferior, because the septal nectary is infralocular; in these species the nectaries have a labyrinthine surface and many vascular bundles. Brocchinia differs from most other fully epigynous species in that each carpel is secretory at the apex and reproductive, rather than secretory, at the base.     

Morphological and molecular phylogenetic context of the angiosperms: contrasting the 'top-down' and 'bottom-up' approaches used to infer the likely characteristics of the first flowers

Recent attempts to address the long-debated 'origin' of the angiosperms depend on a phylogenetic framework derived from a matrix of taxa versus characters; most assume that empirical rigour is proportional to the size of the matrix. Sequence-based genotypic approaches increase the number of characters (nucleotides and indels) in the matrix but are confined to the highly restricted spectrum of extant species, whereas morphology-based approaches increase the number of phylogenetically informative taxa (including fossils) at the expense of accessing only a restricted spectrum of phenotypic characters. The two approaches are currently delivering strongly contrasting hypotheses of relationship. Most molecular studies indicate that all extant gymnosperms form a natural group, suggesting surprisingly early divergence of the lineage that led to angiosperms, whereas morphology-only phylogenies indicate that a succession of (mostly extinct) gymnosperms preceded a later angiosperm origin. Causes of this conflict include: (i) the vast phenotypic and genotypic lacuna, largely reflecting pre-Cenozoic extinctions, that separates early-divergent living angiosperms from their closest relatives among the living gymnosperms; (ii) profound uncertainty regarding which (a) extant and (b) extinct angiosperms are most closely related to gymnosperms; and (iii) profound uncertainty regarding which (a) extant and (b) extinct gymnosperms are most closely related to angiosperms, and thus best serve as 'outgroups' dictating the perceived evolutionary polarity of character transitions among the early-divergent angiosperms. These factors still permit a remarkable range of contrasting, yet credible, hypotheses regarding the order of acquisition of the many phenotypic characters, reproductive and vegetative, that distinguish 'classic' angiospermy from 'classic' gymnospermy. The flower remains ill-defined and its mode (or modes) of origin remains hotly disputed; some definitions and hypotheses of evolutionary relationships preclude a role for the flower in delimiting the angiosperms. We advocate maintenance of parallel, reciprocally illuminating programmes of morphological and molecular phylogeny reconstruction, respectively supported by homology testing through additional taxa (especially fossils) and evolutionary-developmental genetic studies that explore genes potentially responsible for major phenotypic transitions.