Gerhard Prenner

A new subfamily classification of the leguminosae based on a taxonomically comprehensive phylogeny

The classification of the legume family proposed here addresses the long-known non-monophyly of the traditionally recognised subfamily Caesalpinioideae, by recognising six robustly supported monophyletic subfamilies. This new classification uses as its framework the most comprehensive phylogenetic analyses of legumes to date, based on plastid matK gene sequences, and including near-complete sampling of genera (698 of the currently recognised 765 genera) and ca. 20% (3696) of known species. The matK gene region has been the most widely sequenced across the legumes, and in most legume lineages, this gene region is sufficiently variable to yield well-supported clades. This analysis resolves the same major clades as in other phylogenies of whole plastid and nuclear gene sets (with much sparser taxon sampling). Our analysis improves upon previous studies that have used large phylogenies of the Leguminosae for addressing evolutionary questions, because it maximises generic sampling and provides a phylogenetic tree that is based on a fully curated set of sequences that are vouchered and taxonomically validated. The phylogenetic trees obtained and the underlying data are available to browse and download, facilitating subsequent analyses that require evolutionary trees. Here we propose a new community-endorsed classification of the family that reflects the phylogenetic structure that is consistently resolved and recognises six subfamilies in Leguminosae: a recircumscribed Caesalpinioideae DC., Cercidoideae Legume Phylogeny Working Group (stat. nov.), Detarioideae Burmeist., Dialioideae Legume Phylogeny Working Group (stat. nov.), Duparquetioideae Legume Phylogeny Working Group (stat. nov.), and Papilionoideae DC. The traditionally recognised subfamily Mimosoideae is a distinct clade nested within the recircumscribed Caesalpinioideae and is referred to informally as the mimosoid clade pending a forthcoming formal tribal and/or cladebased classification of the new Caesalpinioideae. We provide a key for subfamily identification, descriptions with diagnostic charactertistics for the subfamilies, figures illustrating their floral and fruit diversity, and lists of genera by subfamily. This new classification of Leguminosae represents a consensus view of the international legume systematics community; it invokes both compromise and practicality of use.

The key role of morphology in modelling inflorescence architecture

Emerging evidence suggests that certain key genes control the branching patterns of flower-bearing axes (i.e. inflorescences) in angiosperms. However, the terminology surrounding inflorescence architecture is heavily typological and suffers from radically divergent definitions of terms that together reduce the value of some recent predictive models. We attempt to resolve the paradox of conflicting definitions of the same terms and clarify the assumptions surrounding this complex subject. We argue in favour of uniform terminology and against over-simplification. The valid conceptual platforms for modelling should be clearly defined and should adequately reflect observed structural diversity.

The Asymmetric Androecium in Papilionoideae (Leguminosae): Definition, Occurrence, and Possible Systematic Value

The androecium of Papilionoideae generally consists of 10 stamens in two whorls, with alternating initials, i.e., a monosymmetric androecium. Recent studies show that the concept that regards staminal fusion as a synapomorphy in Papilionoideae has to be abandoned. Thus, reconsidering the importance of these androecial features is necessary, and new morphological characters are needed for a better understanding of legume evolution. In this context, the floral development in 31 species from 15 papilionoid tribes was analyzed by SEM, focusing on androecial symmetry. Together with the analysis of 33 herbarium specimens and the literature, androecial characters of 91 taxa of 27 tribes (of 30 total) are considered. The inner stamen whorl is initiated asymmetrically in 39 species of 11 tribes of Papilionoideae and in some taxa of Caesalpinioideae. The asymmetry is manifested in that the adaxial antepetalous stamen is formed to the left or right of the median plane. In contrast to this, in 52 species of 19 tribes the androecium is initiated symmetrically, with the adaxial stamen lying exactly in the median plane. Asymmetric androecia were found in basal lineages of Papilionoideae as well as in the dalbergioids and parts of genistoids. Bossiaeeae, Genisteae, and Sophoreae show both androecium types, while in taxa of the derived Millettieae‐Phaseoleae and in Hologalegina only symmetric androecia were found. Both androecium types occur independently of staminal fusion and are therefore seen as an interesting “new” androecial character in Papilionoideae. The occurrence of asymmetric androecia in basal lineages of Papilionoideae and in some Caesalpinioideae and its independence from staminal fusion is of interest in understanding legume evolution. I suggest the following hypotheses on the evolution of asymmetric androecia, which are not mutually exclusive: (1) symmetric androecia are derived within Papilionoideae, and/or (2) asymmetry arose independently several times.

THE BRANCHING STAMENS OF RICINUS AND THE HOMOLOGIES OF THE ANGIOSPERM STAMEN FASCICLE

On the basis of new ontogenetic data and a modern phylogenetic context, we reevaluate the nature of the highly unusual branched stamen of Ricinus communis, specifically whether it represents a telomic shoot‐derived (axial) structure or a classical foliar‐derived stamen that is compound or fascicled. Partly independent from the two previous hypotheses, we also discuss whether the Ricinus stamen could represent a reduced flower or inflorescence, as in several other Euphorbiaceae that possess an obscure flower‐inflorescence boundary. Early ontogeny resembles that of other polyandrous Euphorbiaceae (Mercurialis and Dalechampia) and other Malphigiales, such as Hypericum, indicating that the Ricinus stamen is an extended fascicle. In contrast to stamen fascicles of other angiosperms, internodal elongation in Ricinus occurs in the regions between the various individual elements (nodes) of the fascicle, and the entire fascicle is clear of the floral axis. Spontaneous natural stamen terata are possible indicators of a tendency for loss of determinacy in stamens of other Euphorbiaceae. Within angiosperms, stamen fascicles have evolved in parallel several times, in both eudicots and monocots. A predisposition to this specialized type of fascicled polyandry can be found in eudicots; this is clearly nonhomologous with the nonfascicled polyandry of early‐divergent angiosperms.

FLORAL ONTOGENY IN CALLIANDRA ANGUSTIFOLIA (LEGUMINOSAE: MIMOSOIDEAE: INGEAE) AND ITS SYSTEMATIC IMPLICATIONS

The floral ontogeny of Calliandra angustifolia, studied using SEM, shows striking differences compared with all other investigated Mimosoideae. The initiation of the sepals is unidirectional from an adaxial to abaxial position, which is a very rare character within Leguminosae. Aestivation of the calyx is cochlear descending, which is a new character within Ingeae. The synchronous initiation of the petals and their valvate aestivation are the only characters that are congruent with the other studied Mimosoideae. The initiation of the androeceum is helical, which has never been found within Mimosoideae. The early pistil development resembles that of Zapoteca, which was recently segregated from Calliandra, whereas the middle and late developmental stages differ clearly in formation of a sessile pistil without a gynophore and an expanded capitate stigma. The presented character combination is unique within Mimosoideae, and no parallels to the genus Zapoteca could be found.

Myrteae phylogeny, calibration, biogeography and diversification patterns: Increased understanding in the most species rich tribe of Myrtaceae.

Myrteae (c. 2500 species; 51 genera) is the largest tribe of Myrtaceae and an ecologically important groups of angiosperms in the Neotropics. Systematic relationships in Myrteae are complex, hindering conservation initiatives and jeopardizing evolutionary modelling. A well-supported and robust phylogenetic hypothesis was here targeted towards a comprehensive understanding of the relationships within the tribe. The resultant topology was used as a base for key evolutionary analyses such as age estimation, historical biogeography and diversification rate patterns. One nuclear (ITS) and seven chloroplast (psbA-trnH, matK, ndhF, trnl-trnF, trnQ-rps16, rpl16 and rpl32-trnL) DNA regions for 115 taxa representing 46 out of the 51 genera in the tribe were accessed and analysed using maximum likelihood and Bayesian inference tools for phylogenetic reconstruction. Dates of diversification events were estimated and contrasted using two distinct fossil sets (macro and pollen) in BEAST. The subsequent dated phylogenies were compared and analysed for biogeographical patterns using BioGeoBEARS and diversification rates using BAMM. Myrteae phylogeny presents strong statistical support for three major clades within the tribe: Australasian group, Myrtus group and Main Neotropical Lineage. Dating results from calibration using macrofossil are an average of 20 million years older and show an early Paleocene origin of Myrteae, against a mid-Eocene one from the pollen fossil calibration. Biogeographic analysis shows the origin of Myrteae in Zealandia in both calibration approaches, followed by a widespread distribution throughout the still-linked Gondwana continents and diversification of Neotropical endemic lineages by later vicariance. Best configuration shift indicates three points of acceleration in diversification rates, all of them occurring in the Main Neotropical Lineage. Based on the reconstructed topology, several new taxonomic placements were recovered, including: the relative position of Myrtus communis, the placement of the Blepharocalyx group, the absence of generic endemism in the Caribbean, and the paraphyletism of the former Pimenta group. Distinct calibration approaches affect biogeography interpretation, increasing the number of necessary long distance dispersal events in the topology with older nodes. It is hypothesised that biological intrinsic factors such as modifications of embryo type and polyploidy might have played a role in accelerating shifts of diversification rates in Neotropical lineages. Future perspectives include formal subtribal classification, standardization of fossil calibration approaches and better links between diversification shifts and trait evolution.

Morphology, development and homologies of the perianth and floral nectaries in Croton and Astraea (Euphorbiaceae-Malpighiales)

New observations are presented on the ontogeny, vasculature and morphology of both staminate and pistillate flowers of Croton and Astraea. These data support earlier hypotheses that the filamentous structures in pistillate flowers represent reduced and transformed petals. Staminate flowers of both genera possess five free nectaries, which are vascularised by divergences of the sepal traces in Croton and unvascularised in Astraea. In pistillate flowers, there are five separate non-vascularised nectaries in Astraea, but in Croton there is a single nectariferous disk that is vascularised by divergences of the sepal traces. The nectaries are initiated late in floral development, but their location indicates that they could represent the outer stamen whorl transformed into secretory staminodes. Other glandular structures occur in pistillate flowers of most Croton species, resulting in flowers with two secretory organ whorls. In these cases, the inner whorl is formed by modified staminodes. Our observations support the recent segregation of Astraea species from the larger genus Croton. Despite strong similarities between the two genera, there are clear structural differences, including the presence of colleters in Astraea (absent in Croton), moniliform trichomes on petals (rather than simple trichomes in Croton), non-vascularised nectaries (vascularised in Croton) and reduced, non-secretory filamentous structures (well developed and secretory in Croton).

FLORAL EVOLUTION IN THE DETARIEAE (LEGUMINOSAE): PHYLOGENETIC EVIDENCE FOR LABILE FLORAL DEVELOPMENT IN AN EARLY-DIVERGING LEGUME LINEAGE

Premise of research. We examine floral evolution and phylogenetic relationships in the monophyletic Detarieae and related lineages of Caesalpinioideae. Tribe Detarieae (82 genera) includes nearly half of the genera in subfamily Caesalpinioideae and represents some of the most diverse legumes with respect to floral morphology. Methodology. A total of 67 floral ontogenetic and morphological characters were combined with DNA sequences from the plastid trnL-F and matK regions of 34 Detarieae species and representatives of Cassieae, Cercideae, Caesalpinieae, Papilionoideae, and Mimosoideae, for which we have near-complete ontogenetic series. The morphological and ontogenetic characters were optimized onto the resulting most parsimonious phylogenetic trees and Bayesian topology to study character evolution. Pivotal results. Our study supports previously proposed relationships within the tribe Detarieae and among caesalpinioid lineages and indicates that certain features (bracteole and hypanthium characters, sepal initiation, anther position in bud, overlap in timing of initiation of organ whorls) are phylogenetically informative for particular clades whereas others (reductions in petal and stamen number, sepal and petal initiation patterns) have evolved multiple times in parallel in the Detarieae and other Caesalpinioideae. These analyses suggest that modifications that occur early in ontogeny can be good phylogenetic characters for distinguishing both major taxonomic groups and more closely related taxa and that morphological differences that differentiate species within genera can be caused by changes that occur at all stages of ontogeny. Phylogenetic distribution of character states and ontogenetic evidence suggest that in the Caesalpinioideae, loss or suppression of organs within a whorl, both of which are very common, usually does not affect development in subsequent whorls. Conclusions. Our analyses reveal several switches from zygomorphy to actinomorphy (and vice versa), but in Caesalpinioideae (contrary to Papilionoideae), zygomorphy is likely not clearly associated with higher diversification rates. This study suggests that floral initiation patterns are much more variable in Caesalpinioideae than in the other two subfamilies. Although particular patterns may be canalized in certain lineages of the subfamily (Cercideae, Caesalpinieae), in other clades (Detarieae, Dialiinae) floral development is more labile, explaining the high diversity in floral morphology encountered overall in the paraphyletic Caesalpinioideae.

Papilionoid inflorescences revisited (Leguminosae-Papilionoideae)

BACKGROUND AND AIMS The inflorescence structure determines the spatiotemporal arrangement of the flowers during anthesis and is therefore vital for reproductive success. The Leguminosae are among the largest angiosperm plant families and they include some important crop plants. In papilionoid legumes, the raceme is the most common type of inflorescence. However, a range of other inflorescence types have evolved via various developmental processes. A (re-)investigation of inflorescences in Swainsona formosa, Cicer arietinum, Abrus precatorius, Hardenbergia violacea and Kennedia nigricans leads to new insights into reduction mechanisms and to a new hypothesis on the evolution of the papilionoid pseudoraceme. METHODS Inflorescence morphology and ontogeny were studied using scanning electron microscopy (SEM). KEY RESULTS The inflorescence in S. formosa is an umbel with a rare type of pendulum symmetry which may be triggered by the subtending leaf. Inflorescences in C. arietinum are reduced to a single flower. An early formed adaxial bulge is the sterile apex of the inflorescence (i.e. the inflorescence is open and not terminated by a flower). In partial inflorescences of A. precatorius, the axis is reduced and its meristem is relocated towards the main inflorescence. Flower initiation follows a peculiar pendulum pattern. Partial inflorescences in H. violacea and in K. nigricans show reduction tendencies. In both taxa, initiated but early reduced bracteoles are present. CONCLUSIONS Pendulum symmetry in S. formosa is probably associated with distichous phyllotaxis. In C. arietinum, strong reduction tendencies are revealed. Based on studies of A. precatorius, the papilionoid pseudoraceme is reinterpreted as a compound raceme with condensed lateral axes. From an Abrus-like inflorescence, other types can be derived via reduction of flower number and synchronization of flower development. A plea is made for uniform usage of inflorescence terminology.

Is LEAFY a useful marker gene for the flower–inflorescence boundary in the Euphorbia cyathium?

The flower-like reproductive structure of Euphorbia s.l. (Euphorbiaceae) is widely believed to have evolved from an inflorescence, and is therefore interpreted as a special type of pseudanthium, termed a cyathium. However, fuzzy morphological boundaries between the inflorescence, individual flowers, and organs have fuelled the suggestion that the cyathium does not merely superficially resemble a flower but could actually share developmental genetic pathways with a conventional flower. To test this hypothesis, immunolocalizations of FLORICAULA/LEAFY (LFY), a protein associated with floral identity in many angiosperm species, were performed in developing cyathia of different species of Euphorbia. Expression of the LFY protein was found not only in individual floral primordia (as predicted from results in the model organisms Arabidopsis and Anthirrhinum), but also in the cyathium primordium and in the primordia of partial male inflorescences. These results provide further evidence that the evolution of floral traits in pseudanthial inflorescences often involves expression of floral development genes in the inflorescence apex. This finding blurs the conventional rigid distinction between flowers and inflorescences.