Comparative floral development and evolution in tribe Caesalpinieae (Leguminosae: Caesalpinioideae). Haematoxylum

Floral organogenesis and development of the tropical legume trees Haematoxylum campechianum (logwood) and H. brasiletto (brazilwood) were studied using scanning electron microscopy. The aims were to compare ontogenies, and to elucidate the relationships of Haematoxylum with other genera of Caesalpinieae, the basal tribe of Caesalpinioideae. Flowers of Haematoxylum are in racemes or fascicles, lack bracteoles, and are pentamerous, hermaphroditic, and either actinomorphic or zygomorphic. Whorls arise in acropetal order except for the carpel, which arises concurrently with the outer stamens. Sepal order is bidirectional (a rare condition) within the whorl in both. Petals and outer stamens are initiated bidirectionally in H. campechianum, and unidirectionally in H. brasiletto. Inner stamens are initiated unidirectionally in both. In H. campechianum, time of petal initiation overlaps with that of outer stamens, and initiation of the two stamen whorls overlap. In both, the gynoecium becomes stipitate, and a hypanthium forms late in development. Both show many plesiomorphic states at anthesis; H. brasiletto alone shows several specialized states (expressed late in development), including a fused, gibbous calyx cup, a zygomorphic corolla, lightly aggregated filaments held together by hairs, and fenestrations in the stamen column. Ontogenetic divergence late in ontogeny characterizes differences at anthesis between related species.     

Trends in evolution of floral ontogeny in Cassia sensu stricto,Senna, and Chamaecrista (Leguminosae: Caesalpinioideae: Cassieae: Cassiinae); a study in convergence

Distinctions in floral ontogeny among three segregate genera (Cassia sensu stricto, Chamaecrista, and Senna) of Cassia L. support their separation. In all species studied, the order of floral organ initiation is: sepals, petals, antesepalous stamens plus carpel, and lastly antepetalous stamens. Sepal initiation is helical in all three genera, which however differ in whether the first sepal is initiated in median abaxial position (Senna), or abaxial and off-median (Cassia javanica), a rare character state among legumes. Order of petal initiation varies: helical in Senna vs. unidirectional in Cassia and Chamaecrista. Both stamen whorls are uniformly unidirectional. Intergeneric ontogenetic differences occur in phyllotaxy, inflorescence architecture, bracteole formation, overlap of initiation among organ whorls (calyx/corolla in Cassia; two stamen whorls in Chamaecrista), eccentric initiation on one side of a flower, anther attachment, anther pore structure, and precocious carpel initiation in Senna. The asymmetric corolla and androecium in Chamaecrista arise by precocious organ initiation on one side (left or right). The poricidal anther character can result from differing developmental pathways: lateral slits vs. sealing of lateral sutures; clasping hairs vs. sutural ridges; terminal pores (one or two) vs. none; and clamp layer formation internally that prevents lateral dehiscence. Genera differ in corolla aestivation patterns and in stigma type. Convergence is shown among the three genera, based on intergeneric dissimilarities in early floral ontogeny (floral position in the inflorescence, bracteole presence, position of the first sepal initiated, order of petal initiation, asymmetric initiation, overlap between whorls, anther morphology, and time of carpel initiation) resulting in similarities at anthesis (showy, mostly yellow salverform flowers, heteromorphic stamens, poricidal anther dehiscence, bee pollination, and chambered stigma).     

Floral development in the legume tree Colophospermum mopane, Caesalpinioideae: Detarieae

Floral ontogeny of Colophospermum mopane (Kirk ex Benth.) Kirk ex J. Leonard, an apetalous member of the Crudia group with four sepals and a large number (20–25) of stamens, was studied as part of a larger project on reproductive biology of this much-utilized tree. The flowers have been described as being inserted in the axil of a bract, but lacking lateral bracteoles. Four outer, light cream or white 'sepals' are present. The first two sepals are initiated in a lateral position, where the bracteoles, if present, develop in other members of the Caesalpinioideae. The inner sepals arise simultaneously adaxially and abaxially. These four structures, conventionally regarded as sepals, enclose the bud. The outer two 'sepals' should be regarded as lateral bracteoles inserted at the apex of the pedicel. The inner structures represent the only two sepals. The large number of stamens arise on a large meristematic surface and different whorls were not observed. The filaments elongate within the bud and after anthesis become exposed outside the flowers. The filaments are of equal length and the large anthers form a suspended cluster. One carpel develops terminally and gives rise to an indehiscent one-seeded fruit.     

Floral ontogeny in Dialiinae (Caesalpinioideae: Cassieae), a study in organ loss and instability

The Caesalpinioideae are widely variable in their floral ontogeny, and among caesalpinioids, members of the polyphyletic tribe Cassieae are particularly diverse. Within the Cassieae, the monophyletic Dialiinae clade is also marked by a high degree of organ loss, particularly in the largest genus, Dialium. The purpose of this work is to explore the ontogeny of several previously undocumented species of the diverse Dialiinae clade, with the goal of building a more complete picture of floral development and evolution in this group and especially within Dialium. We have documented the floral ontogeny of six species of the Dialiinae; four from Dialium, as well as Poeppigia procera and Mendoravia dumaziana. Mode and timing of organ initiation were mostly consistent across the Dialium species studied. With the exception of Dialium dinklagei, which undergoes helical calyx initiation, all flowers initiated sepals bidirectionally. In the instances of both gains and losses of floral organs in Dialium, one trend is apparent — an absence of abaxial organs. Gains in both sepals and stamens occur in the adaxial median position, while stamens and petals which are lost are always the ventral-most organs. Organ initiation in Poeppigia and Mendoravia is unlike that seen in Dialium. Poeppigia shows a ventral to dorsal unidirectional sepal initiation, while both Poeppigia and Mendoravia display near-synchronous initiation of the corolla and staminal whorls. The taxa examined here exemplify the apparent lack of developmental canalisation seen in caesalpinioid legumes. This ontogenetic plasticity is reflective of the morphological diversity shown by flowers across the subfamily, representing what has been described as an “experimental” phase in legume floral evolution.     

Floral development in Tribe Detarieae (Leguminosae: Caesalpinioideae): Amherstia, Brownea, and Tamarindus

Floral development was compared among three taxa in caesalpinioid tribe Detarieae sensu lato: Amherstia nobilis and Tamarindus indica have racemose, helically arranged inflorescences, while Brownea latifolia has cauliflorous capitate flower clusters that arise as racemes. All have acropetal flower order; initiation and development are sequential in all except Brownea, which is synchronous. All have paired persistent showy bracteoles. Floral symmetry is dorsiventral (zygomorphic) in all except Brownea, with radial symmetry at anthesis. Sepals initiate helically on a circular floral apex, starting with a median abaxial sepal, in all. Petals are initiated helically in Brownea, and unidirectionally in Amherstia and Tamarindus. Stamens are initiated unidirectionally in each stamen whorl in all except Amherstia, in which the outer whorl is bidirectional. The carpel initiates concurrently with the petals in Brownea, and with the outer stamens in the other taxa. The two upper (adaxial) sepal primordia become fused during development in all, so that the calyx appears tetramerous. Some reduced petals occur in Amherstia and Tamarindus, and some reduced stamens occur in all. All produce a hypanthium by zonal growth, and all except Tamarindus have the gynoecium attached adaxially to the hypanthial rim.     

Floral ontogeny in Scirpus, Eriophorum and Dulichium (Cyperaceae), with special reference to the perianth

BACKGROUND AND AIMS: Based on molecular phylogenetic analysis, it has been suggested recently that the Cyperaceae comprises only two subfamilies: the Mapanioideae and the Cyperoideae. In most flowers of the Cyperoideae, the whorl of inner stamens is reduced, resulting in tetracyclic flowers. In the more primitive (scirpoid) genera within the Cyperoideae, the perianth consists of two polysymmetric whorls, whereas the perianth parts in the more derived genera have been subject to modifications and/or reduction. Comparative studies of the many silky hairs of Eriophorum and of the eight bristles of Dulichium have given rise to much discussion about their homology. METHODS: The spikelet and floral ontogeny in freshly collected inflorescences was investigated using scanning electron microscopy. KEY RESULTS: Complete floral ontogenies are presented for Scirpus sylvaticus L., Eriophorum latifolium Hoppe and Dulichium arundinaceum (L.) Britton, with special reference to the perianth. The results in S. sylvaticus confirm the trimerous monocot-like organization of the flower. It is used as a model for floral development in Cyperoideae. In the early developmental stages, the androecium of E. latifolium is surrounded by a massive perigonial primordium, from which the many hair-like bristles originate. Consequently, the stamens develop among the hair primordia, more or less simultaneously. The hairs are arranged in whorls, which develop centripetally. The development of the perianth in D. arundinaceum starts with the formation of three initial perianth primordia opposite the stamens. Subsequently, two more abaxial bristle primordia, alternating with the stamens, originate simultaneously with the appearance of three adaxial bristle primordia in the zone where an adaxial inner perianth primordium is expected. CONCLUSIONS: The floral development in E. latifolium and D. arundinaceum can be considered as variations upon the scirpoid floral ontogenetic theme.     

Floral ontogeny in Dipterygeae (Fabaceae) reveals new insights into one of the earliest branching tribes in papilionoid legumes

Flowers of Dipterygeae (Fabaceae, Papilionoideae) exhibit an unusual petaloid calyx. The two adaxial sepals are large and petaloid, and the three abaxial sepals form a three‐toothed lobe. The goal of this study was to elucidate the ontogenetic pathways of this peculiar calyx in light of the floral development of the three genera that comprise the tribe. Floral buds of Dipteryx alata, Pterodon pubescens and Taralea oppositifolia were analysed using scanning electron microscopy and light microscopy. The order of bracteole and sepal initiation varies among the species. The androecium is asymmetric. The carpel cleft is positioned to the right or to the left, and is opposite the adaxial antepetalous stamen. The peculiarity of the calyx becomes noticeable in the intermediate stages of floral development. It results from the differential growth of the sepal primordia, in which the abaxial and lateral primordia remain diminutive during floral development, compared with the adaxial ones that enlarge and elongate. Bracteoles, abaxial sepals, petals and anthers are appendiculate, except in T. oppositifolia, in which the appendices were not found in bracteoles or anthers. These appendices comprise secretory canals or cavities. Considering that the ontogenetic pathway for the formation of the petaloid calyx is similar and exclusive for Dipterygeae, it might be a potential synapomorphy for the group, with the presence of secretory canals in the appendices of abaxial and lateral sepals and petals. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174 , 529–550.     

Development of megagametophyte, embryo, and seed in Senna corymbosa (Lam.) H.S. Irwin & Barneby (Leguminosae – Caesalpinioideae)

The main aspects of seed ontogeny in Senna corymbosa were studied by standard anatomical microtechniques for light microscope observations. The results revealed an ana-campylotropous, bitegmic, and crassinucelate mature ovule. A single archesporocyte developed by an archesporial cell enlargement from the subhypodermal multicellular archesporium. Meiosis originated linear or T-shaped megasporic tetrads. The functional megaspore was the chalazal one. Megagametophytic development conformed to the Polygonum type. Fertilization was porogamic. Endosperm development was free nuclear and conformed to a chalazal haustorium. Cellular endosperm was initiated from the micropylar end during the globular embryo stage. Embryogeny derived from a linear proembryonal tetrad. The mature embryo showed an oblique axis. The testa derived from the outer ovular integument. Nucellar and endosperm remnants, and the micropylar region of the inner ovular integument, persisted at embryo maturity. The absence of a pleurogram would be adaptative to wetland habitats. The taxonomic use of the mature embryo axis in the Cassieae and the phylogenetic employment of megasporic arrangements in Leguminosae needs some reinterpretation.  © 2007 The Linnean Society of London, Botanical Journal of the Linnean Society , 2007, 153 , 169–179.     

Evolutionary loss of sepals and/or petals in detarioid legume taxa Aphanocalyx, Brachystegia, and Monopetalanthus (Leguminosae: Caesalpinioideae)

Floral development using scanning electron microscopy is compared in several taxa of the Brachystegia subtribal group of caesalpinioid tribe Detariae. This group is characterized by missing sepals and/or petals. In Aphanocalyx djumaensis, Monopetalanthus durandii, and two Brachystegia species, one sepal is initiated in median abaxial position. In the first two, one or two additional sepal rudiments may initiate late. Brachystegia species have all five sepals, which remain scalelike. In Aphanocalyx and Monopetalanthus, one petal initiates adaxially and medianly (a position atypical for the first initiated petal in the family); additional petal rudiments may form in lateral sites. In Brachystegia, five petals are initiated unidirectionally on a meristem ring, but all are suppressed after initiation. In all taxa, ten stamens are initiated on a ring meristem: unidirectionally in Monopetalanthus, bidirectionally in Brachystegia, vs. in erratic order in Aphanocalyx. Carpel and petal initiation are concurrent. Different organ whorls overlap in time in Monopetalanthus and Brachystegia. In all, the floral apex characteristically is elongate radially and narrow tangentially after bracteole initiation. Two ontogenetic features, the meristem ring and the radially elongate post-bracteole floral apex, appear to be possible synapomorphies for the Brachystegia group.     

Floral ontogeny in ficinia and isolepis (cyperaceae), with focus on the nature and origin of the gynophore

BACKGROUND AND AIMS: The generic delimitations of Ficinia and Isolepis, sister genera in the Cypereae, are blurred. Typical Ficinia flowers have a lobed gynophore, which envelops the base of the nutlet, whereas in Isolepis the character is considered to be absent. Some former species of Isolepis, lacking the gynophore, were recently included in Ficinia. The floral ontogeny of representative taxa in Ficinia and Isolepis were investigated with the aim of evaluating the origin and nature of the gynophore in the Cypereae. METHODS: The spikelet and floral ontogeny in inflorescences collected in the field was investigated using scanning electron microscopy (SEM) and light microscopy (LM). KEY RESULTS: SEM images of Isolepis setacea and I. antarctica, Ficinia brevifolia, F. minutiflora, F. zeyheri and F. gracilis, and LM sections of F. radiata, show that the gynoecium in Ficinia is elevated above the flower receptacle by the development of a hypogynous stalk. From its apex, a (often three-)lobed cup is formed, which envelopes the basal part of the later nutlet. In developing flowers of I. antarctica, a rudimentary hypogynous stalk appears. In I. setacea, rudiments of a hypogynous stalk can be observed at maturity. In F. radiata and F. zeyheri, intralocular hairs are present in the micropylar zone. At the surface of developing gynoecia in flowers of F. gracilis, star-shaped cuticular structures appear which disappear again at maturity. CONCLUSIONS: The overall floral ontogeny of all species studied occurs following a typical scirpoid pattern, though no perianth primordia are formed. The gynophore in Ficinia originates as a hypogynous stalk, from which the typical gynophore lobes develop. The gynophore is not homologous with the perianth.     

Pseudoracemes in papilionoid legumes: their nature, development, and variation

Pseudoracemes in papilionoid legumes: their nature, development, and variation. Cymelike partial inflorescences called fascicles have been reported in the inflorescences of several papilionoid tribes. The total inflorescence is termed a ‘pseudoraceme’ because of the multiple flowers in each bract axil. Pseudoraceme development has been studied in 22 taxa in five papilionoid tribes (Abreae, Desmodieae, Millcttieae, Phaseoleae and Psoraleeae). Two to twelve flowers occur per bract axil among various taxa, with three the most common number.Pongamia pinnata and Clitoris fairchildiana have only two flowers per axil; Vigna radiata, Phaseolus vulgaris, and Apios americana have four to five commonly, and Dioclea aff.ucayalina and Abrus precalorius have up to 12. The ‘fascicle’ usually consists of a triad of three flowers; each triad resembles a dichasial cyme in that the middle flower appears terminal. The middle flower however is subtended by a bract on the abaxial side, so that the middle flower is technically lateral. When the first-order axis elongates, each triad may either remain intact or be separated by axis intervalS. Many variations on the basic triad pattern occur in the species studied: 1.one or two flowers may develop while others that are initiated remain suppressed; 2. Additional flowers may be produced that replicate the first triad; 3. Additional flowers may form medianly only, on the abaxial side. The second-order inflorescence axis which has produced the three flowers persists to produce more flowers in replication of the triad pattern in several taxa (Apios americana, Vigna radiata, Phaseolus vulgaris, and Dioclea aff.ucayalina). In Butea monosperma the second-order inflorescence apex produces subsequent flowers (after the triad) in a helix. In Erylhrina perrieri, there is no indication of a persistent second-order inflorescence apex after the central flower; such a condition could be interpreted as a cyme, except for the abaxial subtending bract. The triad in Psoralea pinnata is a true cyme; the middle flower lacks a subtending bract other than that subtending the entire fascicle. Developmentally, the difference between a cyme and an early-determinate raceme (as in the triad type of pseudoraceme) is rather slight. Comparison of the types of inflorescences described here may indicate how the transition may have occurred between racemes and cymes in the evolution of legumes.     

Floral ontogeny in tribe Dalbergieae (Leguminosae: Papilionoideae):Dalbergia brasiliensis, Machaerium villosum s. l.Platymiscium floribundum, andPterocarpus rotundifolius

Floral organogenesis and development of the tropical legume treesDalbergia brasiliensis, Machaerium villosum, Platymiscium floribundum, andPterocarpus rotundifolius were studied using scanning electron microscopy. The aims were to compare ontogenies and to elucidate if floral ontogenetic data will provide new character states diagnostic of the tribe Dalbergieae, which is considered a basal papilionoid tribe and primarily defined on fruit characters. Organ inception is principally acropetal in all taxa studied. Carpel inception is, however, consistently precocious. InD. brasiliensis sepals are initiated in an order not previously reported in Papilionoideae. It may be considered modified helical. InP. rotundifolius the inner whorl of stamens initiate in an unusual way, this is lateral two stamens first, then the two abaxial ones, and last the adaxial one, opposed to the unidirectional order usually seen in Papilionoideae. Generally the differences in flower development among the studied genera appear at initiation and late stage in ontogenesis, rather than at mid-stage.     

Floral ontogeny, pattern formation, and evolution in Hibbertia and Adrastaea (Dilleniaceae)

Floral development was compared with scanning electron microscopy in 12 Australian species of Hibbertia representing most of its morphological variation, and in the related Adrastaea (Dilleniaceae). Calyx and corolla arise in quincuncial helices in radially symmetrical species, while the petals initiate unidirectionally from one side in zygomorphic species. Stamen number (3-200+) proliferates by centrifugal addition of individual primordia or by innovations of common primordia and ring meristems. Common primordia arise in single-stamen positions alternately with petals, and each produces one to several stamens centrifugally that remain attached to a shared base and form a stamen fascicle. A ring meristem in Adrastaea initiates a whorl of five stamens, alternate with the first stamens but outside their whorl. In radially symmetrical species of Hibbertia, a first ring of stamens is supplemented centrifugally by additional stamens on a meristem ring. The first stamens in zygomorphic species of Hibbertia initiate as a terminal ridge on the floral apex, with subsequent stamens added centrifugally on one side and two carpels initiated on the opposite side. The carpels arise as a simultaneous ring in radially symmetrical flowers, or as a simultaneous pair in zygomorphic species. Staminodial presence is viewed as of minor significance. Four pollinator syndromes are proposed for Hibbertia, related to differing floral architecture.     

Does the relative importance of resource competition and architectural effect in floral variation vary with stages of floral ontogeny?

Variation in floral allocation within inflorescences has been attributed to resource competition and/or architectural effect.The two hypotheses were extensively studied and both hypotheses were partly ...     

Proliferating Floral Organs (Pfo), a Lotus japonicus gene required for specifying floral meristem determinacy and organ identity,encodes an F-box protein

To study flower development in the model legume Lotus japonicus, a population of transgenic plants containing a maize transposable element (Ac) in their genome was screened for floral mutants. One mutation named proliferating floral organs (pfo) causes plants to produce a large number of sepal-like organs instead of normal flowers. It segregates as a single recessive Mendelian locus, and causes sterility. Scanning electron microscopy revealed that pfo affects the identity, number and arrangement of floral organs. Sepal-like organs form in the first whorl, and secondary floral meristems are produced in the next whorl. These in turn produce sepal-like organs in the first whorl and floral meristems in the second whorl, and the process is reiterated. Petals and stamens are absent while carpels are either absent or reduced. The pfo phenotype was correlated with the presence of an Ac insertion yielding a 1.6-kb HindIII restriction fragment on Southern blots. Both the mutant phenotype and this Ac element are unstable. Using the transposon as a tag, the Pfo gene was isolated. Conceptual translation of Pfo predicts a protein containing an F-box, with high overall similarity to the Antirrhinum FIMBRIATA, Arabidopsis UNUSUAL FLORAL ORGANS and Pisum sativum Stamina pistilloida proteins. This suggests that Pfo may regulate floral organ identity and meristem determinacy by targeting proteins for ubiquitination.     

Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). 2. Zygomorphic taxa with petal and stamen suppression

Marked floral zygomorphy and a reduced number of petals and/or stamens are the character traits that distinguish the taxa described (species of Afzelia, Berlinia, Gilbertiodendron, Macrolobium, Neochevalierodendron, Paramacrolobium, Phyllocarpus, and Tetraberlinia). All have an "Omega"-shaped floral apex after bracteole initiation, bracteoles large when initiated, helical sepal initiation, unidirectional petal initiation (simultaneous in Afzelia, not determinable in Tetraberlinia), and unidirectional stamen initiation. Floral zygomorphy is expressed primarily by one petal being much larger than the others and by suppression of several of the stamens. Five petals are initiated in all; suppression begins in late development. Either two petals (Neochevalierodendron, Phyllocarpus) or four petals (Afzelia, Berlinia, Macrolobium, Tetraberlinia) are suppressed. All ten stamens are initiated; at midstage, suppression begins in either three stamens (Afzelia) or seven stamens (Gilbertiodendron, Macrolobium, Paramacrolobium). Other expressions of zygomorphy may include diadelphy, stamen filament connation late in development, or displacement of the carpel from a central position to the adaxial side of the hypanthium. There is no loss of organs similar to that which occurs in some other Detarieae.     

Martiodendron fluminense (Leguminosae, Caesalpinioideae), a new species from the Atlantic coast rainforest of Brazil

A new species of Leguminosae is described and illustrated:Martiodendron fluminense, the southernmost and the only species of the genus to occur in the Atlantic forests of southeastern Brazil.     

Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). 1. Radially symmetrical taxa lacking organ suppression

Flowers in detarioid legume taxa (Isoberlinia angolensis, Microberlinia brazzavillensis, M. bisulcata, Hymenostegia klainii) initiate all 21 floral organs, are radially symmetrical, and have little or no organ suppression. All share a narrow, "Omega"-shaped floral apex and massive bracteoles at initiation. All have helical sepal initiation, starting abaxially. They differ in whether the first sepal initiates medianly (Microberlinia brazzavillensis, M. bisulcata) or nonmedianly (Isoberlinia angolensis, Hymenostegia klainii), and in petal order: helical (I. angolensis) or unidirectional (M. brazzavillensis, M. bisulcata, H. klainii). Stamens initiate in unidirectional order in each whorl except in M. brazzavillensis, which has a bidirectional outer whorl. An unusual feature is the ring meristem in M. bisulcata, on which petals and stamens are initiated. Overlap in time of organ initiation between whorls occurs in I. angolensis, M. brazzavillensis, and M. bisulcata but not in H. klainii. The carpel initiates concurrently with petals in all except H. klainii, in which it initiates with the outer stamens. The carpel remains open at ovule initiation in both species of Microberlinia. These detarioid taxa represent elements of the tribe having essentially radially symmetrical flowers, with all organs initiated and persisting to anthesis, but their specialized "Omega" character-state complex is shared with specialized taxa that have zygomorphic flowers and some organs suppressed.