Comparative inflorescence and floral ontogeny in the genus Mentha (Mentheae: Nepetoideae: Lamiaceae): variable sequences of organ appearance and random petal aestivation

The genus Mentha is a taxonomically complex genus, characterized by large morphological variations. Only a few, frequently overlapping, characters are of value in taxonomy. Comparative floral developmental studies provide an opportunity for better understanding the systematic relationships among different species. The inflorescence and floral ontogeny of three Mentha L. species (M. piperita L., M. pulegium L. and M. suaveolens Ehrh.) were investigated using epi-illumination light microscopy. All three species studied have thyrses with the same developmental pathway. The lack of higher order bracts and the monochasial branching of the higher order inflorescence apices were found as special features of inflorescence ontogeny. Sepals appear unidirectionally from the adaxial side in all except for M. pulegium which shows a modified unidirectional sequence. Variable sequences of petal and stamen appearance from unidirectional to reversed unidirectional sequence are present in all. Significant ontogenetic features include (1) appearance of the corolla as a rim before petal lobes become visible and (2) instability in petal aestivation. Morphological features including densely hairy calyx, five-lobed corolla tube, smaller adaxial stamens and hairy ovary with included style distinguish M. pulegium from the other species. On the basis of our results floral ontogenetic features could be considered important characters for delimiting or diagnosing different sections in the genus Mentha. Variable sequences of petal lobe appearance and instability in petal aestivation were found as unusual developmental characters.     

PATTERNS OF FLORAL DEVELOPMENT IN AGALINIS AND ALLIES (SCROPHULARIACEAE). II. FLORAL DEVELOPMENT OF AGALINIS DENSIFLORA

Initiation of floral primordia begins in Agalinis densiflora with production of two lateral adaxial calyx lobe primordia followed by a midadaxial primordium, and then primordia of two abaxial calyx lobes. Initiation of three abaxial corolla lobe primordia is succeeded by that of two stamen pairs and then by primordia of two adaxial corolla lobes. The primordium of the abaxial carpel appears before the adaxial one. Except for the calyx, initiation of primordia proceeds unidirectionally from the abaxial to the adaxial side of the floral apex. Zygomorphy in the calyx, corolla, and androecium is evident during initiation of primordia and is accentuated during organogenesis. The calyx undergoes comparatively rapid organogenesis, but the inner three floral series undergo a protracted period of organogenesis. The perianth series reach maturation prior to meiosis in the anthers. Maturation of the androecium and gynoecium are postmeiotic events.     

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 CAESALPINIA (LEGUMINOSAE)

Utilizing scanning electron microscopy, we studied the early floral ontogeny of three species of Caesalpinia (Leguminosae: Caesalpinioideae): C. cassioides, C. pulcherrima, and C. vesicaria. Interspecific differences among the three are minor at early and middle stages of floral development. Members of the calyx, corolla, first stamen whorl, and second stamen whorl appear in acropetal order, except that the carpel is present before appearance of the last three inner stamens. Sepals are formed in generally unidirectional succession, beginning with one on the abaxial side next to the subtending bracts, followed by the two lateral sepals and adaxial sepal, then lastly the other adaxial sepal. In one flower of C. vesicaria, sepals were helically initiated. In the calyx, the first-initiated sepal maintains a size advantage over the other four sepals and eventually becomes cucullate, enveloping the remaining parts of the flower. The cucullate abaxial sepal is found in the majority of species of the genus Caesalpinia. Petals, outer stamens, and inner stamens are formed unidirectionally in each whorl from the abaxial to the adaxial sides of the flower. Abaxial stamens are present before the last petals are visible as mounds on the adaxial side, so that the floral apex is engaged in initiation of different categories of floral organs at the same time.     

The development of pistillate and perfect florets in Xeranthemum squarrosum (Asteraceae)

The formation of capitulum inflorescence with two different types of floret is an interesting issue in floral biology and evolution. Here we studied the inflorescence, floral ontogeny and development of the everlasting herb, Xeranthemum squarrosum, using epi‐illumination microscopy. The small vegetative apex enlarged and produced involucral bracts with helical phyllotaxy, which subtended floret primordia in the innermost whorl. Initiation of floret primordia was followed by an acropetal sequence, except for pistillate peripheral florets. The origin of receptacular bracts was unusual, as they derived from the floral primordia rather than the receptacular surface. The order of whorl initiation in both disc and pistillate flowers included corolla, androecium and finally calyx, together with the gynoecium. The inception of sepals and stamens occurred in unidirectional order starting from the abaxial side, whereas petals incepted unidirectionally from the adaxial or abaxial side. Substantial differences were observed in flower structure and the development between pistillate and perfect florets. Pistillate florets presented a zygomorphic floral primordium, tetramerous corolla and androecium and two sepal lobes. In these florets, two sepal lobes and four stamen primordia stopped growing, and the ovary developed neither an ovule nor a typical stigma. The results suggest that peripheral pistillate florets in X. squarrosum, which has a bilabiate corolla, could be considered as an intermediate state between ancestral bilabiate florets and the derived ray florets.     

台闽苣苔（苦苣苔科）花部器官的形态发生

在扫描电镜下对台闽苣苔 (T .oldhamii (Hemsl.)Solereder)进行了花部器官形态发生的观察 ,为探索该类群的个体发育、类群间的系统发育关系和进化趋势提供依据。研究发现该属植物萼片、花冠和雄蕊发生式样均为五数花类型 ,它们各自来源于花原基上分化出来的萼片原基、花冠原基和雄蕊原基 ;花冠与雄蕊的两侧对称性与花冠上唇生长稍快和退化雄蕊原基发育迟滞相关 ;萼片原基的发生和发育的顺序是不一致的 :萼片原基发生的式样为近轴中原基—远轴 2原基— 2侧原基 ,发育式样则为近轴中萼片— 2侧萼片—远轴 2萼片 ,花蕾时为镊合状排列。花冠裂片原基的发生和发育式样是一致的 ,即远轴中裂原基 (下唇中裂片 )—远轴 2侧裂原基 (下唇 2侧裂片 )—近轴 2裂原基 (上唇 2裂片 )。花蕾期卷迭式为覆瓦状排列 ,从外向内 :下唇中裂片—下唇 2侧裂片—上唇 2裂片或下唇 2侧裂片—上唇 2裂片—下唇中裂片。雄蕊原基与花冠裂片原基互生 ,前方雄蕊原基在发生上稍迟于后方雄蕊原基 ,后者与退化雄蕊原基几乎同时发生 ,但较小 ,并与近轴心皮 (或柱头上唇 )对生。将该属与玄参科 (Scrophulari aceae)的地黄属 (Rehmannia)、苦苣苔科 (Gesneriaceae)的异叶苣苔属 (Whytockia)和尖舌苣苔属 (Rhynchoglossum)的花部器官比较发现     

Comparative floral development in the tribe Mentheae (Nepetoideae: Lamiaceae) and its bearing on the evolution of floral patterns in asterids

A comparative developmental study of flowers was carried out using epi-illumination light microscopy on four genera of Lamiaceae (Nepeta, Rosmarinus, Salvia, andZiziphora), representing all three subtribes of Mentheae. All species examined share unidirectional (adaxial to abaxial) sepal initiation, except Rosmarinus, which has the reverse unidirectional sequence, starting abaxially. Initiated but suppressed bracteoles were detected only in Rosmarinus. In Rosmarinus, Salvia, and Ziziphora, initiation of petals and stamens proceeds unidirectionally from the abaxial side. Floral initiation of Nepeta has bidirectional inception of petals and unidirectional stamen initiation from the adaxial side. Temporal overlap in organ initiation between petal and stamen whorls occurs in all taxa, though this feature is more prominent in Rosmarinus. Significant structural and developmental features that distinguish the four genera include: (1) polysymmetric calyx tube, highly tomentose corolla and deeply four-partitioned ovary in Nepeta; (2) monosymmetric two-lipped calyx and shallowly four-partitioned ovary in Ziziphora; and (3) suppression of adaxial stamens in Salvia and Rosmarinus. Adaxial stamens are absent from Rosmarinus, but reduced stamens remain as staminodia in Salvia. In a phylogenetic context, the late monosymmetry of Nepeta and very early monosymmetry of Rosmarinus could both be regarded as derived conditions compared with the early monosymmetry ofSalvia and Ziziphora.     

Development of the cymose inflorescence, cupulum and flower of Psoralea pinnata (Leguminosae: Papilionoideae: Psoraleeae)

The inflorescence of Psoralea pinnata sensu lato is composed of dichasial cymes of three to seven flowers in each bract axil. However, the main inflorescence terminal is indeterminate. Cymes are very unusual among legumes, occurring in perhaps six or seven genera. The 'cupulum' is a unique structure found only in Psoralea among legumes. While highly variable in form, it serves as a protective structure around the calyx during development. Developmentally the cupulum results from fusion by intercalary growth of three to four successive bracts on the pedicel. Paired bracteoles are also produced above the cupulum and below the calyx, but they are very reduced and easily overlooked. Their presence is evidence that the cupulum is not part of the flower proper. Organogeny in P. pinnata is unidirectional in each floral whorl, starting on the abaxia! side, except for a minor exception in precocity of the vexillary (adaxial) stamen arising with the two lateral stamens of the same inner whorl. There is no overlap between whorls. The carpel is initiated early, during or just after petal initiation and before stamen initiation.     

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 Organogenesis and Development of Two Taxa in Tribe Hyoscyameae (Solanaceae)?aPrzewalskia tangutica and Hyoscyamus niger

Floral organogenesis and development of Przewalskia tangutica Maxim.endemic to China and Hyoscyamus niger L., which belong to the tribe Hyoscyameae (Solanaceae), were studied using scanning electron microscope. They have three common characters of floral organ initiation and development: 1) initiation of the floral organs in the two species follows Hofmeister’s rule; 2) the mode of corolla tube development belongs to the “late sympetaly” type; 3) primordia of the floral appendages initiated in a pentamerous pattern and acropetal order. But initiation of the calyx lobe primordia showed different modes in these two species. The calyx lobe primordia of H. niger have simultaneously whorled initiation, while those of P. tangutica have helical initiation, but the five calyx lobe primordia form a ring after all five calyx lobe primordia occur. The systematic significance of the present results in the genera Hyoscyamus and Przewalskia is discussed in this paper.     

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.     

Patterns and Significance of Floral Development in Whytockia (Gesneriaceae)

Abstract: The floral development of Whytockia W. W. Smith has been studied in order to explore the developmental basis for the arrangement and differentiation patterns of floral organs, and the evolutionary relationship between Whytockia and allies in floral development. The descending imbricate aestivations in both calyx and corolla have remarkably different ontogenetic patterns between calyx and corolla which are derivative with respect to the development of the valvate aestivations in the four-stamened Rhynchoglossum. Both corolla lobes and stamens are initiated simultaneously from the same ring meristem. However, the five stamens remarkably precede the initiation of the five corolla lobes. Also, the adaxial stamen is suppressed after initiation to become a staminode, concomitant with retardation of its adjacent organs during development. This situation, together with the non-acropetal order among whorls of floral organs in Whytockia, is possibly related to a late expression and a remarkably different expression pattern of cycloidea- like genes as compared to Antirrhinum. Furthermore, the axile placentation in the bilocular ovary of Whytockia is formed by an involute closure of carpels rather than derived from a secondary fusion of two intrusive parietal placentae.     

Secretory hairs in Gentiana and allied genera (Gentianaceae, subtribe Gentianinae) from the Iberian Peninsula

Eleven species from six different sections of the genus Gentiana , as well as one species each of genera Gentianella (G. campestris), Gentianopsis (G. ciliata), Comastoma (C. tenellum) and Swertia (S. perennis) have been studied by light microscopy for the presence of hairs in floral as well as in vegetative parts. Hairs are produced in the calyx and vegetative leaves of all of them, and also in the corollae of the last three species. They fall into two different types: those found in the corolla of Gentianopsis ciliata are non-secretory, while in the rest of the species studied, and also in the calyx and leaves of G. ciliata , they produce a mucilaginous secretion. Calycine and foliar hairs are always produced in the adaxial epidermis at the base of the foliar organ, and are considered as mucilage secreting colleters. The presence of colleters in vegetative organs has not been adequately considered in previous taxonomic accounts, in spite of their presumed significance.     

Floral ontogeny in Sophoreae (Leguminosae: Papilionoideae): II. Sophora sensu lato (Sophora group)

Floral ontogeny is described in eight species of Sophora sensu lato, representing the Sophora group, as part of a comparative ontogenetic analysis of Polhill's eight groups of tribe Sophoreae, subfamily Papilionoideae. This tribe includes taxa having relatively unspecialized floral structure. Flowers have a five-lobed calyx, a corolla of five free petals, ten mostly unfused, identical stamens, and a carpel. Order of initiation is predominantly acropetal (except for the carpel): sepals, petals, outer stamens plus carpel, inner stamens. Order of initiation within each whorl is unidirectional from the abaxial side. Overlapping initiation among whorls occurs only in S. chrysophylla. Keel petals are slightly fused in six species, and wing petals are fused in 5. tomentosa. Two bird-pollinated species (S. chrysophylla, S. microphylla) lack the papilionaceous corolla of other species, and their petals are unusually long and lack wing sculpturing found in the others. Other floral differences among species mostly involve flower color, differing absolute or relative sizes among organs, and degree of reflexing of vexillum. All but S. davidii have a hypanthium, which develops very late, starting when the bud is about 5 mm long. The distinctions among species (petal size, degree of reflexed position of vexillum, petal sculpturing, color, anther shape, filament hairs, hypanthium presence, calyx lobing) tend to be expressed late in ontogeny.     

Floral anatomy of the Lecointea clade (Leguminosae, Papilionoideae, Swartzieae sensu lato)

Flower and inflorescence anatomy and morphology of Exostyles, Harleyodendron, Holocalyx, Lecointea, and Zollernia (Leguminosae, Lecointea clade) were studied. Features common to all genera but otherwise rare within the Leguminosae include: (1) the presence of phenolic compounds in the epidermal cells of the anthers and subepidermal cells of the bracteoles, sepals, petals, and ovaries (absent in Holocalyx balansae); (2) simple trichomes on the adaxial base of the bracteoles and on the surface of the calyx and ovaries; and (3) tapetum persisting until the androspores are formed. Other notable anatomical features are: (1) colleters on the adaxial bases of the bracts and bracteoles of Holocalyx balansae and Zollernia ilicifolia; (2) trichomes on the anthers of Harleyodendron unifoliolatum, Holocalyx balansae, Lecointea hatschbachii, Zollernia ilicifolia and Z. magnifica; (3) osmophores on the petals of Exostyles godoyensis; (4) asynchronous pollen development in the anthers of Holocalyx balansae and Zollernia magnifica; and (5) vascular bundles surrounded by lignified fibers in Harleyodendron unifoliolatum. These anatomical characters are discussed according to their possible phylogenetic implications.     

Early floral development of Pentaphylacaceae (Ericales) and its systematic implications

Early floral development of four species from the genera Anneslea, Cleyera, Eurya, and Ternstroemia of Pentaphylacaceae, was studied comparatively using scanning electron microscopy. Together with earlier studies in Euryodendron and Adinandra, 6 out of 12 genera of Pentaphylacaceae have now been studied for their floral development. The usually pentamerous flowers of these taxa share a number of developmental features: the perianth organs appear in a clockwise or anticlockwise spiral sequence on the floral apex with relatively long plastochrons between successive organs, resulting in conspicuous size differences among perianth organs during early developmental stages. The early development of the usually polystemonous androecium is characterized by an indistinct ring-primordium and a mostly concave floral apex; individual stamens appear subsequently on this ring-primordium. However, further development of the androecium differs conspicuously among taxa and we describe three main developmental patterns for the family including features such as centripetal stamen whorls and stamens fascicles. Unusual features of floral development and organization of Pentaphylacaceae include: (1) a pronounced spiral sequence of organ appearance during early floral development in perianth and androecium; (2) the occurrence of paired organs in the corolla and the androecium of some species; (3) sepals and petals that are positioned opposite from each other in the genera Anneslea and Ternstroemia; and (4) a concave floral apex at the beginning of androecium development. From a systematic point of view our results clearly support a close relationship between Anneslea and Ternstroemia and also suggest a closer relationship among Adinandra, Cleyera, and Euryodendron on the one hand and between Eurya and Visnea on the other. Further, our developmental study stresses the differences between Pentaphylacaceae and Theaceae, which earlier where thought to form a natural group of plants. While high stamen numbers are achieved via centripetal pattern of stamen formation in the former family, stamens are formed centrifugally in the latter.     

Ipomopsis sancti-spiritus (Polemoniaceae), a new species from northern New Mexico

Ipomopsis sancti-spiritus, a new species in sect.Ipomopsis, from the mountains of northern New Mexico is described and illustrated. The purplish calyx, pink corolla, and a short pistil with the stigma situated below the included stamens represent a unique combination of characters. The new species is similar toI. arizonica but differs primarily in corolla color and in length of the pistil.     

FLORAL MORPHOLOGY,ORGANOGENESIS AND INTERPRETATION OF THE INFERIOR OVARY IN DOWNINGIA BACIGALUPII

The inflorescence of Downingia bacigalupii (Campanulaceae; Lobelioideae) is an indeterminate spike. Axillary flowers have a long, linear, inferior ovary with parietal placentation, a pentamerous synsepalous calyx, zygomorphic sympetalous corolla, syngenesious stamens, and a bicarpellate, syncarpous gynoecium. On the basis of floral vascular anatomy the inferior ovary is interpreted as appendicular, representing adnation of outer floral whorls to the gynoecium. Floral ontogeny shows that sepals are initiated in an adaxial to abaxial sequence rather than the 2/5 phyllotaxis reported for other members of Lobelioideae. Growth of the common bases of sepal lobes forms a floral cup and initiation of the following floral whorls occurs along the inner margins of the cup. Continued basal growth of the cup-shaped bud results in the formation of the elongated inferior ovary. Earlier evidence for the interpretation of a cup-shaped receptacle during development of epigynous flowers is reexamined and it is concluded that the concave floral bud of D. bacigalupii can also be interpreted as common growth of connate floral whorls, supporting interpretations based on vascular anatomy. Comparison of floral development between Downingia bacigalupii and Pereskia aculeata (Cactaceae) reveals ontogenetic differences between flowers with appendicular and receptacular cups.     

Floral structure, development and diversity in Thunbergia (Acanthaceae)

Floral structure and development of 18 species of Thunbergia (Thunbergioideae si , Acanthaceae) were studied comparatively. The flowers of Thunbergia are highly diverse and show a wide range of pollination syndromes. In general they are large and showy. Their pollination apparatus is highly elaborate, floral organs are often synorganized, and floral architecture is complex. In contrast to the high diversity of the anthetic flowers, their bauplan is uniform and their early development shows no major differences, i.e. in all species studied, the calyx arises as a ring primordium, the corolla is 'late sympetalous', and petals and stamens are initiated more or less simultaneously. Some differences are found in further calyx development, where several developmental patterns are present. More significant differences arise only later during development and mainly concern the structures of the calyx, the anthers, the stigma, and corolla aestivation. In the anthetic flowers there are many special characters that are present in all or the majority of the species studied, e.g. the calyx is reduced, the corolla tube is subdivided into two compartments and the anthers lack an endothecium. The present results on development and morphology of the flowers of Thunbergia are compatible with an earlier subdivision of the genus into eight subgenera.