Dmitry D. Sokoloff

A taxonomic nightmare comes true: phylogeny and biogeography of glassworts (Salicornia L., Chenopodiaceae)

In this study we analysed ETS sequence data of 164 accessions belonging to 31 taxa of Salicornia, a widespread, hygrohalophytic genus of succulent, annual herbs of Chenopodiaceae subfam. Salicornioideae, to investigate phylogenetic and biogeographical patterns and hypothesise about the processes that shaped them. Furthermore, our aim was to understand the reasons for the notorious taxonomic difficulties in Salicornia. Salicornia probably originated during the Miocene somewhere between the Mediterranean and Central Asia from within the perennial Sarcocornia and started to diversify during Late Pliocene/Early Pleistocene. The climatic deterioration and landscape-evolution caused by orogenetic processes probably favoured the evolution and initial diversification of this annual, strongly inbreeding lineage from the perennial Sarcocornia that shows only very limited frost tolerance. The further diversification of Salicornia was promoted by at least five intercontinental dispersal events (2 x to South Africa, at least 3 x to North America) and at least two independent polyploidization events resulting in rapidly expanding tetraploid lineages, both of which are able to grow in lower belts of the saltmarshes than their diploid relatives. The diploid lineages of Salicornia also show rapid and effective range expansion resulting in both widespread genotypes and multiple genotypes in a given area. Reproductive isolation through geographical isolation after dispersal, inbreeding, and comparatively young age might be responsible for the large number of only weakly differentiated lineages. The sequence data show that the taxonomic confusion in Salicornia has two major reasons: (1) in the absence of a global revision and the presence of high phenotypic plasticity, the same widespread genotypes having been given different names in different regions, and (2) striking morphological parallelism and weak morphological differentiation led to the misapplication of the same name to different genotypes in one region.

EVOLUTIONARY HISTORY OF THE MONOCOT FLOWER

Abstract This paper reviews monocot flower structure and gynoecium development and evaluates these data to clarify the evolutionary history of the monocot flower. Despite some congruence between molecular and morphological data regarding the delimitation and phylogenetic relationships of monocots, there is currently no universally accepted view on the morphology of the ancestral monocot flower, reflecting a high degree of parallelism in monocot floral evolution. We focus on two character suites that encompass the key features of monocot flowers: (1) the typical monocot groundplan of trimerous-pentacyclic flowers, and (2) a character suite related to carpel fusion, including postgenital fusion between carpels and the presence of septal nectaries. It is likely that the trimerous-pentacyclic flower represents a major synapomorphy of monocots; this flower groundplan is virtually absent from the closest relatives of monocots. Such close correlation of a particular groundplan with a phylogenetic group is analogous with the absence of the typical eudicot flower groundplan in basal eudicots, though in both instances the underlying constraints are obscure. In monocots, morphogenetic studies and analysis of character correlations lead us to favor a hypothesis that the ancestral monocot conditions were postgenital fusion between carpels and presence of septal (gynopleural) nectaries. This character-suite optimization contrasts with optimizations of individual morphological characters, which suggest that the ancestral monocot flower possessed congenitally united carpels (with no contribution of postgenital fusion) and lacked septal nectaries. Among extant early divergent monocots, flowers of Japonolirion Nakai (Petrosaviaceae s.l. or Japonoliriaceae, Petrosaviales) appear to most closely resemble those of the ancestral monocots. A gynoecium with free carpels represents a derived condition in monocots; it evolved independently in three unrelated groups (Triuridaceae, Arecaceae, Alismatales), with several gains of apocarpy in Alismatales and palms. All three monocot groups that include free-carpellate species show significant variation in their individual floral groundplans.

Seed fertilization, development, and germination in Hydatellaceae (Nymphaeales): Implications for endosperm evolution in early angiosperms.

New data on endosperm development in the early-divergent angiosperm Trithuria (Hydatellaceae) indicate that double fertilization results in formation of cellularized micropylar and unicellular chalazal domains with contrasting ontogenetic trajectories, as in waterlilies. The micropylar domain ultimately forms the cellular endosperm in the dispersed seed. The chalazal domain forms a single-celled haustorium with a large nucleus; this haustorium ultimately degenerates to form a space in the dispersed seed, similar to the chalazal endosperm haustorium of waterlilies. The endosperm condition in Trithuria and waterlilies resembles the helobial condition that characterizes some monocots, but contrasts with Amborella and Illicium, in which most of the mature endosperm is formed from the chalazal domain. The precise location of the primary endosperm nucleus governs the relative sizes of the chalazal and micropylar domains, but not their subsequent developmental trajectories. The unusual tissue layer surrounding the bilobed cotyledonary sheath in seedlings of some species of Trithuria is a belt of persistent endosperm, comparable with that of some other early-divergent angiosperms with a well-developed perisperm, such as Saururaceae and Piperaceae. The endosperm of Trithuria is limited in size and storage capacity but relatively persistent.

Flower structure and development in Tupidanthus calyptratus (Araliaceae): an extreme case of polymery among asterids

Flowers of Tupidanthus show an extreme case of floral polymery among asterids. Floral development and gynoecium structure have been examined. The floral meristem has a complex folded shape. The tiny calyx is initiated as a continuous ring primordium. The corolla is initiated as a lobed ring and develops into a calyptra. All stamen primordia appear simultaneously as a single whorl. The carpels, also in a single whorl, tend to alternate with the stamens. Some Schefflera species related to Tupidanthus are also studied. The flower of Tupidanthus is interpreted as a result of fasciation. Further investigation should determine whether mutation(s) in gene(s) of the CLAVATA family are responsible for the fasciation here. The significance of Tupidanthus for understanding spatial pattern formation in flowers of Araliaceae, and both functional and developmental constraints in angiosperm flowers with a single polymerous carpel whorl are discussed.

Comparative pollen morphology in the early-divergent angiosperm family Hydatellaceae reveals variation at the infraspecific level

The small aquatic family Hydatellaceae was recently assigned to the early‐divergent angiosperm order Nymphaeales. Pollen morphology is described using both SEM and LM for all 12 species of Hydatellaceae, and using TEM for one species (T. submersa). These observations are compared with pollen data from the other two families of Nymphaeales, Nymphaeaceae and Cabombaceae, including original observations for both genera of Cabombaceae. No significant interspecific variation in pollen morphology occurs in Hydatellaceae, though both of the perennial species (Trithuria inconspicua and T. filamentosa), which could be apomictic, possess at least partially sterile and collapsed pollen. Pollen of Trithuria is small, oblong or rounded (viewed from the distal pole) and monosulcate. The aperture has a distinct margin and extends the full length of the pollen grain. The exine is tectate‐columellate. The tectum is perforate: discontinuous with numerous small perforations randomly scattered over the entire non‐apertural surface. The exine surface is microechinate. In most species of Trithuria, a small percentage of pollen grains possess a trichotomosulcate aperture. In two species, rare atypical grains with striate or partially striate exine sculpturing were found. This striate pattern is very similar to exine sculpturing in Gymnotheca (Saururaceae, Piperales). The presence of anasulcate pollen does not contradict placement of Hydatellaceae within Nymphaeales, but this pollen type is also common among other early‐divergent angiosperms and monocots. Exine sculpturing differs between Cabombaceae, Hydatellaceae and Nymphaeaceae, but this character also differs between the two genera of Cabombaceae and among genera of Nymphaeaceae. Compared with other families of Nymphaeales, Hydatellaceae are relatively uniform in pollen morphology.

Evolution of the monocot gynoecium: evidence from comparative morphology and development in Tofieldia, Japonolirion, Petrosavia and Narthecium

We present new comparative morphological and developmental data on gynoecia of three genera of early-divergent monocots: Tofieldia (Tofieldiaceae, Alismatales), Petrosavia and Japonolirion (Petrosaviaceae, Petrosaviales) and one lilioid monocot: Narthecium (Nartheciaceae, Dioscoreales). Our data show significant differences between the genera examined, and are congruent with the splitting of former Nartheciaceae sensu Tamura (1998) into families Tofieldiaceae, Petrosaviaceae NB-cosistent with later and Nartheciacae (APG II 2003). Our investigation confirms the presence of at least partial carpel fusion in all taxa examined. Previous data indicating apocarpy in Japonolirion, some Petrosavia and Tofieldia could be due to late postgenital carpel fusion in these plants. Syncarpy also characterises other early-divergent monocot lineages such as Acoraceae and Araceae. It is most parsimonious to regard syncarpy as a primitive condition for monocots, but an alternative scenario suggests that apocarpy is plesiomorphic among monocots, involving multiple origins of syncarpy. The latter hypothesis is supported by significant differences between gynoecia of early-divergent monocots, including different modes of carpel fusion.

Inflorescence and Early Flower Development in Loteae (Leguminosae) in a Phylogenetic and Taxonomic Context

Molecular phylogeny shows that the temperate legume tribe Loteae is close to the mostly tropical Robinieae and monogeneric Sesbanieae, but comparative morphological studies of these groups are limited. Unusual patterns of inflorescence symmetry and calyx development have been described in some Loteae, but taxon sampling was low. We studied these features with scanning electron microscopy in 25 species of Loteae plus in three Robinia species. Phylogenetic trees of Loteae based on nuclear ribosomal ITS sequences and 77 morphological characters are constructed. Our data show that whorled flower arrangement is a synapomorphy of Loteae; joint initiation of the two adaxial sepals is a synapomorphy of a clade containing Hippocrepis, Scorpiurus, and Coronilla; floral buds bent backward early in development are a synapomorphy of Coronilla; bilateral umbel symmetry and the presence of a single whorl of flowers are probably primitive within Loteae. Inflorescences of Robinia show no special similarities with those of Loteae. Developmental data support homologies between sterile bracts in all Loteae. Even if the sterile bract is situated at the top of the peduncle, it is morphologically the first leaf on the peduncle. Monosymmetric umbels of Loteae (including the model legume Lotus japonicus) could be useful for investigating genetic control of symmetry in structures of hierarchic levels higher than flowers.

Unique stigmatic hairs and pollen-tube growth within the stigmatic cell wall in the early-divergent angiosperm family Hydatellaceae

BACKGROUND AND AIMS The ultrastructure of the pollen tubes and the unusual multicellular stigmatic hairs of Trithuria, the sole genus of Hydatellaceae, are described in the context of comparative studies of stigmatic and transmitting tissue in other early-divergent angiosperms. METHODS Scanning and transmission electron microscopy and immunocytochemistry are used to study the structure and composition of both mature and immature stigmatic hair cells and pollen-tube growth in Trithuria. KEY RESULTS Trithuria possesses a dry-type stigma. Pollen tubes grow within the cell walls of the long multicellular stigmatic hairs. Immunocytochemistry results suggest that arabinogalactan proteins are involved in attracting the pollen tubes through the stigmatic cuticle. Most tubes grow along the hair axis towards its base, but some grow towards the hair apex, suggesting that pollen tubes are guided by both physical constraints such as microfibril orientation and the presence of binding factors such as unesterified pectins and adhesive proteins. CONCLUSIONS The presence of a dry-type stigma in Trithuria supports the hypothesis that this condition is ancestral in angiosperms. Each multicellular stigmatic hair of Hydatellaceae is morphologically homologous with a stigmatic papilla of other angiosperms, but functions as an independent stigma and style. This unusual combination of factors makes Hydatellaceae a useful model for comparative studies of pollen-tube growth in early angiosperms.

Morphology and development of the gynoecium in Centrolepidaceae: the most remarkable range of variation in Poales.

This paper explores the relative impacts of reduction and polymerization on the evolution of reproductive structures in the small but morphologically diverse family Centrolepidaceae. Centrolepidaceae are closely related to Restionaceae and belong to the large order Poales, which also includes the grasses. In the largest genus of Centrolepidaceae, Centrolepis, the reproductive structures are viewed either as highly unusual aggregations of reduced flowers (the pseudanthial interpretation) or as unique flowers evolved through extreme reduction in the androecium, usually accompanied by a drastic increase in carpel number and elaboration of the entire gynoecium. Comparative data are here presented on gynoecia of all three genera of Centrolepidaceae; these data strongly support the latter (euanthial) interpretation. The combined phenomenon of carpel multiplication and decrease in stamen number is unexpected in a predominantly wind-pollinated lineage. Applying a pseudanthial interpretation would create a considerable morphological gap with reproductive structures of other Poales, whereas accepting a euanthial concept allows an almost continuous morphological series with related taxa.

Molecular phylogenetics of Hydatellaceae (Nymphaeales): Sexual-system homoplasy and a new sectional classification

PREMISE OF THE STUDY Species relationships are unknown in Hydatellaceae, a small family of dwarf aquatics related to water lilies that arose near the base of angiosperm phylogeny. Here we use molecular evidence to infer a species tree for the family and apply this to reconstructing major transitions in morphology and sexual system in this early branch of angiosperms. METHODS We assembled plastid (atpB, matK, ndhF, rbcL) and nuclear (ribosomal ITS) data for 50 samples (including outgroups) and estimated a species tree for Hydatellaceae using a Bayesian multispecies coalescent approach. We reconstructed the evolution of several morphological characters, then tested for associations between sexual system and reproductive morphology using phylogenetic ANOVA. KEY RESULTS Dioecious species of Hydatellaceae have significantly greater stamen number and anther length than do cosexual species, suggesting changes in male function. The perennial habit that defines one subclade likely represents a reversion from annuality. Species relationships do not fall along traditional morphological divisions, but new sections proposed here are supported by fruit and seed synapomorphies. The earliest split in the family is reflected in geography and climate (i.e., tropical vs. subtropical/temperate clades). We found limited evidence of incongruence between plastid and nuclear trees, with one exception involving gene-tree nonmonophyly for two close relatives (Trithuria submersa, T. bibracteata). CONCLUSIONS While the direction of sexual-system evolution is ambiguous, transitions are significantly associated with changes in involucral phyllome length and proxies of pollen production. We propose a new sectional circumscription based on fruit, seed, and DNA evidence.