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SEM micrographs of the developmental sequence of Aconitum napellus. (A) Young inflorescence; (B) floral primordium showing the first three sepals (after removal of the bract and of the two prophylls); (C, D) floral primordia showing the spiral initiation of sepals (numbers indicate the order of initiation of sepals); (E) floral primordium showing the second and fifth petals (seventh and tenth perianth members, P7 and P10) initiating in front of the dorsal sepal, and a very young stamen primordium (St); (F-H) floral primordia showing spiral initiation of stamens; (I) basal view of a floral bud showing reduced petals (Rp); (J) side view of a floral bud showing the two spurred petals of different size (P7 and P10); (K) apical view of a floral bud showing three carpels in central position surrounded by stamens; (L) side view of a floral bud showing a spurred petal and stamens. Scale bars: (A-K) ¼ 100 mm; (L) ¼ 1 mm.
Source publication
Ranunculaceae presents both ancestral and derived floral traits for eudicots, and as such is of potential interest to understand key steps involved in the evolution of zygomorphy in eudicots. Zygomorphy evolved once in Ranunculaceae, in the speciose and derived tribe Delphinieae. This tribe consists of two genera (Aconitum and Delphinium s.l.) comp...
Contexts in source publication
Context 1
... symmetry in Ranunculaceae (whether actinomorphic or zygomorphic) is actually imperfect due to spiral initiation (Endress, 1999) and a homogeneous growth resulting in unequal size among organs sharing a same identity [in Aconitum (Fig. 3) and Delphinium (Fig. 5, and Fig. S1 in Supplementary data) the growth of one spurred petal is delayed compared with the other]. This situation is specific to ...
Context 2
... in the three Delphinieae species is established late in development, compared with the situation in the two outgroup species Synaphea spinulosa and Antirrhinum majus, where zygomorphy is established during initiation of the calyx (Douglas, 1997;Vincent and Coen, 2004). In the tribe Delphinieae, the floral apex remains a circular and Interestingly, zygomorphy becomes conspicuous from the outside of the flower still later, when the stalks of the spurred petals begin to grow (Fig. 4), and the dorsal sepal differentiates into a helmet in Aconitum (Figs 3 and 4) and into a single spur in Delphinium (Fig. 5, and Fig. S1 in Supplementary data). It must be noticed that the elongation of the dorsal sepal does not take place simultaneously with that of nectar spurs. Indeed, a phase of latency with a specific duration for each species pre- cedes the formation of the spur or hood in the dorsal sepal (Fig. 2). Spurred petals reach their final length after ...
Context 3
... the early stages of development of the species bearing petals, petal primordia are different from sepal primordia in shape and size. Moreover, the cell type may also help dis- tinguish between both ( Kramer et al., 2007). In contrast, petal primordia are indistinguishable from stamen primordia, exhibiting similar shape and size (Figs 3 and 5, and Fig. S1 in Supplementary data; Payer, 1857;Tepfer, 1953;Hiepko, 1965;Sattler, 1973;Kosuge andTamura, 1988, 1989;Kosuge, 1994). This similarity was also shown at the anatom- ical level (Payer, 1857;Smith, 1928;Hiepko, 1965;Tamura, 1965Tamura, , 1984Erbar et al., 1999). The link of petals with stami- nodes (andropetals) in Ranunculaceae was hypothesized by Ronse De Craene and Smets (1994,1995) and Erbar et al. (1999), based on morphological and developmental obser- vations. Petals in Ranunculaceae were considered as the outer- most whorl of the androecium, and interpreted in a phylogenetic sense as heterotopic staminodes (Ronse De Craene and Smets, 2001;see Ronse De Craene, 2003). An alternative hypothesis has been presented by a recent develop- mental genetic study of Rasmussen et al. (2009). The authors have shown that petals in the whole order Ranunculales must not be seen as homoplastic derived staminodes but rather as the result of a genetic developmental programme, common to Berberidaceae and Ranunculaceae. Gradients of gene expression may lead to the morphological grades ( Kunst et al., 1989) between stamens and petals that were interpreted in the past as reproducing the evolutionary history between stamens and ...
Citations
... The default condition for these organ-specific transitions tends to be from radial to bilateral symmetry. One potent example is in the Aconitum genus (Ranunculaceae family) where the actinormophic (radially symmetric) developing flower transitions towards zygomorphy (bilaterally symmetric) through the development of a petal spur on just one side of the flower [3,57,58]. Symmetry can also be linked to genes related to floral organ identity and growth in the Fumarioideae flower where paralogs to the CRABSCLAW (CRC) gene, a master regulator of gynoecium identity in Arabidopsis [59], and CYC, which is essential for growth control in Antirrhinum [23], are responsible for the shift from biradial symmetry towards a bilateral conformation throughout the development of the flower. Rarely, in plants, do radial-to-bilateral symmetry transitions occur [60]. ...
Flowers are plant structures characteristic of the phylum Angiosperms composed of organs thought to have emerged from homologous structures to leaves in order to specialize in a distinctive function: reproduction. Symmetric shapes, colours, and scents all play important functional roles in flower biology. The evolution of flower symmetry and the morphology of individual flower parts (sepals, petals, stamens, and carpels) has significantly contributed to the diversity of reproductive strategies across flowering plant species. This diversity facilitates attractiveness for pollination, protection of gametes, efficient fertilization, and seed production. Symmetry, the establishment of body axes, and fate determination are tightly linked. The complex genetic networks underlying the establishment of organ, tissue, and cellular identity, as well as the growth regulators acting across the body axes, are steadily being elucidated in the field. In this review, we summarise the wealth of research already at our fingertips to begin weaving together how separate processes involved in specifying organ identity within the flower may interact, providing a functional perspective on how identity determination and axial regulation may be coordinated to inform symmetrical floral organ structures.
... The stamens ( Figure 1a1) are numerous and measure about 10 mm long. The fruit is glabrous, ending in a short bristle, usually with three joined follicles, each follicle with 10-15 seeds and winged edges (Jabbour et al., 2009(Jabbour et al., , 2016. ...
Aconitum napellus L. is a popular medicinal plant extensively used in homeopathy. This article provides detailed morphology and microscopy, including the anatomical and histochemical features of the herb, to aid authentication and quality control. In cross‐section, the root in secondary growth shows the phloem surrounded by pericyclic fibers and a well‐developed xylem. The stem is irregular in outline, displaying unicellular trichomes and many free collateral vascular bundles encircling the pith. The leaf is dorsiventral, hypostomatic with anomocytic and anisocytic stomata, and shows non‐glandular trichomes. The floral parts are characterized by uniseriate epidermises, homogeneous mesophyll, anomocytic stomata on the abaxial surface, trichomes, and oval pollen grains. The tissue fragments in powdered herbs show these characteristics and have numerous starch grains with thimble‐shaped, linear or star‐shaped hilum. The detailed macroscopic and microscopic analysis provided in this study can help in the authentication and quality control of A. napellus raw materials.
Research Highlights
Key anatomical, micromorphological, and microchemical features of Aconitum napellus are described.
The results of the study can support the taxonomy of the genus Aconitum .
Morphological standardization of the species reported here is helpful in the quality control of this herb.
... In Ranunculales, petals of some families are highly elaborate and complex. Spurred petals occur in Berberidaceae (four in Epimedium), Papaveraceae (one in Fumaria and two in Lamprocapnos) and Ranunculaceae (five in Aquilegia and Urophysa; two in Aconitum, Delphinium, Gymnaconitum, and Staphisagria; one in Delphinium subgenus Consolida) (Cronquist 1981, Endress 1995 Ronse De Craene 2007, Jabbour et al. 2009, Zhang et al. 2014, Zhao et al. 2016b, Chang et al. 2019. Within Ranunculaceae, the petals of some genera (Nigella, Trollius, and Xanthorhiza) are elaborate with concealed nectar in spurs and glistening pseudonectaries on the outside, which are formed to attract insects (Weber 1993, Endress 1995, Zhao et al. 2011, Liao et al. 2020. ...
Epimedium and Plagiorhegma are the representatives of two early-diverging clades in Podophylloideae of Berberidaceae. Flowers are dimerous and trimerous respectively, but their floral development is little known. Here, we used scanning electron microscopy to clarify the structure and development of flower and inflorescence in Epimedium pubescens and Plagiorhegma dubium and compared these with other Berberidaceae to better understand floral evolution within the family. Our results show that the two genera share some significant features. The petal and stamen primordia emerge independently. The carpel is ascidiate from the earliest stages of development. The ovule is anatropous and bitegmic. However, E. pubescens has a paniculate inflorescence, while a lateral floral bud is initiated but aborted in P. dubium. In E. pubescens, both inner sepals and petals are delayed compared with other organs (vs. delay in petal development only for P. dubium). Petals of E. pubescens have a nectariferous spur (vs. no nectariferous tissue for P. dubium). The style of E. pubescens is long with a flat stigma (vs. short with trumpet-shaped stigma for P. dubium). These differences suggest that Epimedium and Plagiorhegma may not be closely related and support placing them separately in two clades of Podophylloideae, complementing results from molecular studies.
... It has been shown that CYCLOIDEA (CYC) and its paralog DICHOTOMA (DICH), encoding TCP transcription factors, are involved in the control of zygomorphic flower development in Antirrhinum majus (Luo et al., 1996;Luo et al., 1999). Furthermore, it has been found that CYC-like TCP family proteins have been recruited to play central roles in determining zygomorphy development in different species (Howarth and Donoghue, 2006;Busch and Zachgo, 2007;Broholm et al., 2008;Kim et al., 2008;Hileman and Cubas, 2009;Jabbour et al., 2009;Preston and Hileman, 2009;Rosin and Kramer, 2009;Zhang et al., 2010;Fambrini et al., 2011;Busch et al., 2012;Yang et al., 2012;Yang X. et al.,2015;Citerne et al., 2017;Dong et al., 2018;Hsu et al., 2018;Spencer and Kim, 2018;Zhao et al., 2018;Sengupta and Hileman, 2022;Sun et al., 2022). ...
Broad diversity of flowers in Fabaceae provides a good system to investigate development and evolution of floral symmetry in higher plants. Many studies have demonstrated a conserved mechanism controlling development of zygomorphic flower during last decades. However, the molecular basis of how asymmetric flower established is largely unknown. In this study, we characterized mutants named keeled wings (kw) in mungbean (Vigna radiata L.), which is a legume species with asymmetric flowers. Compared to those in the wild type plants, the lateral petals were ventralized in the kw mutants. Map-based cloning showed that KW was VrCYC3 gene in mungbean, the ortholog of Lotus japonicus CYC3 (LjCYC3) and Pisum sativum CYC3 (PsCYC3). In addition, another two CYC-like genes named VrCYC1 and VrCYC2 were identified from mungbean genome. The three CYC-like genes displayed distinct expression patterns in dorsal, lateral and ventral petals. It was found that VrCYC3 was located in nucleus. Further analysis showed that VrCYC3 had transcription activity and could interact with VrCYC1 and VrCYC2 in yeast cell. Moreover, the deletion of two amino acid residues in the R domain of VrCYC3 protein could decrease its interaction with VrCYC1 and VrCYC2 proteins. Our results suggest that LjCYC3/VrCYC3 orthologs play conserved roles determining the lateral petal shape and identity of zygomorphic flower as well as asymmetric flower in Papilionoideae.
... We chose Aconitum napellus to represent the genus in the ancestral state reconstructions, because in the genus this species has been the most extensively studied regarding morphology, anatomy and development (Kosuge and Tamura, 1988;Erbar et al., 1999;Jabbour et al., 2009). In addition, this species was selected for our developmental study. ...
Ranunculaceae comprise ca. 2,500 species (ca. 55 genera) that display a broad range of floral diversity, particularly at the level of the perianth. Petals, when present, are often referred to as “elaborate” because they have a complex morphology. In addition, the petals usually produce and store nectar, which gives them a crucial functional role in the interaction with pollinators. Its morphological diversity and species richness make this family a particularly suitable model group for studying the evolution of complex morphologies. Our aims are (1) to reconstruct the ancestral form of the petal and evolutionary stages at the scale of Ranunculaceae, (2) to test the hypothesis that there are morphogenetic regions on the petal that are common to all species and that interspecific morphological diversity may be due to differences in the relative proportions of these regions during development. We scored and analyzed traits (descriptors) that characterize in detail the complexity of mature petal morphology in 32 genera. Furthermore, we described petal development using high resolution X-Ray computed tomography (HRX-CT) in six species with contrasting petal forms (Ficaria verna, Helleborus orientalis, Staphisagria picta, Aconitum napellus, Nigella damascena, Aquilegia vulgaris). Ancestral state reconstruction was performed using a robust and dated phylogeny of the family, allowing us to produce new hypotheses for petal evolution in Ranunculaceae. Our results suggest a flat ancestral petal with a short claw for the entire family and for the ancestors of all tribes except Adonideae. The elaborate petals that are present in different lineages have evolved independently, and similar morphologies are the result of convergent evolution.
... In Antirrhinum majus, bilateral symmetry is formed by the arrangement of the upper-dorsal and lower-ventral petals during their allometric growth (Luo et al. 1996). In delphinium plants, the radial symmetry of original flowers transforms into bilateral symmetry due to the rapid growth of sepal and petal at the late developmental stage of floral organ (Jabbour et al. 2009). In addition, the mutual inhibition of growth among different floral organs could lead to the formation of bilateral symmetry by degenerating one or more floral organs during development (Rudall and Bateman, 2004;Mitchell and Diggle 2005). ...
Key message
The overexpression of HaCYC2c and its regulation on HaNDUA2 through transcriptional recognition are important for regulating the heteromorphous development and functional differentiation of ray and disc florets in sunflower.
Abstract
Flower symmetry is closely related to pollinator recruitment and individual fecundity for higher plants and is the main feature used to identify flower type in angiosperms. In sunflower, HaCYC2c regulates floral organ development and floral symmetry, but the specific detail remains unclear. In this study, sunflower long petal mutant (lpm) with HaCYC2c insertion mutation was used to investigate the regulating role of HaCYC2c in the morphogenesis of florets and the transformation of floral symmetry through phenotype, transcriptome, qRT-PCR, and possible protein-gene interactions analyses. Results showed that HaCYC2c was overexpressed after an insertion into the promoter region. This gene could recognize the cis-acting element GGTCCC in the promoter region of HaNDUA2 that might regulate HaNDUA2 and affect other related genes. As a consequence, the abnormal elongation of disc petals and the degradation of male reproductive system occurred at the early development of floral organ in sunflower. Furthermore, this insertion mutation resulted in floral symmetry transformation, from actinomorphy to zygomorphy, thereby making the tubular disc florets transformed into ray-like disc florets in sunflower lpm. The findings suggested that the overexpression of HaCYC2c and its control of HaNDUA2 through transcriptional recognition might be an important regulating node of the heteromorphous development and functional differentiation for ray and disc florets in sunflower. This node contributes to the understanding of the balance between pollinator recruitment capacity of ray florets and fertility of disc florets for the optimization of reproductive efficiency and enhancement of species competitiveness in sunflower.
... In the early-diverging eudicot family Ranunculaceae, a large diversity of petal forms is found, from simple laminas with a tiny nectariferous scale, as in Ranunculus, to highly elaborate nectariferous spurred organs, as in Aquilegia. Floral development and, to a lesser extent, petal development have already been described qualitatively using the classical microscopy techniques (Erbar et al., 1999;Tucker and Hodges, 2005;Jabbour et al., 2009Jabbour et al., , 2015Ren et al., 2009;Zhao et al., 2011). A detailed investigation of the development of the elaborate petal has been conducted in the genus Nigella using histology and micro-CT (Yao et al., 2019). ...
Petals, the inner organs in a differentiated perianth, generally play an important role in pollinator attraction. As such they exhibit an extraordinary diversity of shapes, sizes, and colors. Being involved in pollinator attraction and reward, they are privileged targets of evolution. The corolla of the Ranunculaceae species Nigella damascena consists of elaborate nectariferous petals, made of a stalk, upper, and lower lips forming a nectar pouch, shiny pseudonectaries, and pilose ears. While the main events of petal development are properly described, a few is known about the pattern of organ size and shape covariation and the cellular dynamics during development. In this study, we investigated the relationships between morphogenesis and growth of N. damascena petals using geometric morphometrics coupled with the study of cell characteristics. First, we found that petal shape and size dynamics are allometric during development and that their covariation suggests that petal shape change dynamics are exponentially slower than growth. We then found that cell proliferation is the major driver of shape patterning during development, while petal size dynamics are mostly driven by cell expansion. Our analyses provide a quantitative basis to characterize the relationships between shape, size, and cell characteristics during the development of an elaborate floral structure. Such studies lay the ground for future evo-devo investigations of the large morphological diversity observed in nectariferous structures, in Ranunculaceae and beyond.
... Zygomorphy evolved only once in the family, in the lineage leading to Delphinieae (25% of all species of Ranunculaceae). Studies of trait evolution in a phylogenetic context have shown that the transition to zygomorphy was associated with perianth structure modification and the acquisition of nectar spurs (Jabbour et al., 2009(Jabbour et al., , 2012b(Jabbour et al., , 2014. Delphinieae include four genera, namely Staphisagria Hill, Aconitum L., Gymnaconitum (Stapf) Wei Wang & Z.D. Chen and Delphinium L. (Jabbour & Renner, 2012a;Wang et al., 2013; and are sister to Nigelleae (Zhai et al., 2019). ...
... Studies of floral morphology and development in several genera and subgenera of Delphinieae (Jabbour et al., 2009;Jabbour & Renner, 2012b;Wang et al., 2013;Espinosa et al., 2017;Chang et al., 2019) have greatly contributed to a better understanding of the evolution of flower structure within the tribe. In Delphinieae, eight petal primordia are initiated in an ontogenic spiral, and depending on petal development and position generally develop into three types of petals [absent only in the peloric D. ecalcaratum S.Y. ...
... The Fp, also called lateral petal, 0.8-1.0 × 0.4-0.6 cm, is dolabriform or ovate, bilobed, with a base subtruncate or broadly cuneate, and a helically twisted (see below) stalk (2-3 mm). The Rp, called a staminode by some authors (Kosuge & Tamura, 1989;Erbar, Kusma & Leins, 1998) or more generally ventral petal (Jabbour et al., 2009), is hardly observable due to its arrested development at an early stage. Occasionally, some Rp can develop to some extent into slender petaloid structures (Supporting Information, Fig. S1). ...
Delphinieae (Ranunculaceae) are characterized by zygomorphic spiral flowers and show a remarkable diversity of perianth organization. Floral structure and development have been investigated in most lineages of the tribe, mainly focusing on the establishment of symmetry and on perianth development. In this study, floral organogenesis and morphogenesis in Delphinium anthriscifolium, a member of the recently erected Delphinium subgenus Anthriscifolium, were investigated and compared with those of other species of Delphinieae in a phylogenetic context. In D. anthriscifolium, zygomorphy of the spiral flower is established soon after the initiation of sepal primordia. Among the four fully developed petals of the dorsoventralized corolla, the two dorsalmost ones become spurred, and the lateral petals resupinate before anthesis and are mirror images of each other. Resupination of petals, long overlooked in morphological studies of Delphinieae, is here reported in Ranunculaceae for the first time. The role of resupinated petals, possibly acting as a landing platform for nectar foragers, may be of high adaptive significance. Based on our new findings regarding floral ontogeny and morphology in D. anthriscifolium, we provide an updated picture of floral evolution in Delphinieae.
... f. (Tamura 1993;Keener et al. 1999;Turland and Barrie 2001;Jabbour and Renner 2011a, b). Zygomorphic flowers and the presence of diterpene alkaloids turned out to be the synapomorphies to this taxonomic group (Johansson 1995;Jabbour et al. 2009Jabbour et al. , 2014. Genus Aconitum consists of the following monophyletic subgenera: subg. ...
In this article, we present a revised taxonomic circumscription of Aconitum subg. Aconitum (Ranunculaceae) in Europe. In total, the subgenus contains some 250 species with the major center of diversity in Eastern Asia. Altogether 94 taxa (species and infraspecific taxa, including hybrids) occur in Europe. Among them, 22 are native species, and 28 are nothospecies (including hybrid formulae). The research is based on former (since Linnaeus) and recent species diagnoses integrating herbarium and field studies carried out in the Alps, Carpathians, Balkans, Spanish Sierra Nevada, Sudetes, and Corsica. The subgenus includes three sections in Europe: the diploid sect. Cammarum, the tetraploid sect. Aconitum, and the monospecific, allopolyploid sect. Angustifolium. Additionally, a triploid, hybridogenous nothosection Acomarum (sect. Aconitum × sect. Cammarum) is presented. For each species, type citation, a concise morphological description, including infraspecific variation and hybridization, geographical distribution, and iconography sources are given. Also, a key to the determination of all taxa is presented. The proposed system scrutinizes former and recent species concepts and gives a base for further studies on the genus’ phylogeny and biotechnology.
... The two dorsalmost are spurred and nectariferous, and the pair of petal spurs is nested within the spur or hood of the dorsal sepal (for more details about Delphinieae floral organization, see Jabbour and Renner 2012b). Floral morphology in Delphinieae has been the object of numerous studies, mostly focusing on spurred petal morphology and development (Payer 1857;Kosuge andTamura 1988, 1989;Erbar et al. 1998;Jabbour et al. 2009; Jabbour and Renner 2012b; W. Zhang, Y. Liu, T. Nie, C. Guo, L. Qiu, G. Yang, F. Jabbour, and W. Wang, unpublished manuscript). According to Endress (2001), a spur is a hollow outgrowth of a laminar organ. ...
... 2F) stops soon after initiation. This developmental delay observed in the petals is common in Ranunculaceae (Payer 1857;Jabbour et al. 2009;Zhao et al. 2011Zhao et al. , 2012 and is also a feature of other plant families (Payer 1857;Sattler 1973). ...
... and developmental scenarios presented here are updated versions of those presented by Jabbour and Renner (2012b) and Jabbour et al. (2009), respectively. ...
Premise of the research. Floral synorganization is a structural feature of many speciose angiosperm taxa, and is considered as a morphological innovation paving the way for evolutionary diversification. Staphisagria is sister to the remaining Delphinieae, the only lineage of Ranunculaceae characterized by zygomorphic flowers. We aim at providing a description of floral organogenesis and morphogenesis in both Staphisagria species, presenting the disparity of Delphinieae hyperorgan in a phylogenetic framework, and proposing a scenario of likely developmental pathways underlying the different types of hyperorgans in Delphinieae.
Methodology. We carried out morphological, anatomical, and developmental studies on flowers of Staphisagria macrosperma and S. picta. Pivotal results. Synorganization is complex in Staphisagria and Delphinieae as a whole, and involves flower dorsoventralization, nesting of spurs, postgenital fusion of petals, and the formation of a shared cavity. From a choripetalous ancestor, late and partial postgenital fusion among dorsal petals evolved once or twice in the tribe.
Conclusions. Delphinieae flower includes nested spurs and nested floral parlors. These key innovations, unique in angiosperms, probably led to the diversification of this species-rich tribe in the Northern Hemisphere. The length of the inner (nectariferous) spurs and the nested floral parlors determine the range of pollinators able to collect nectar. These traits could be used to revise the circumscription of taxonomic groups within the tribe, and should be taken into account when examining the possible coevolution between Delphinieae flowers and their pollinators. Integrating this new knowledge about the hyperorgan will be essential for future research in taxonomy, evo-devo and pollination ecology in Delphinieae.
