Testing the ontogenetic base for the transient model of inflorescence development

Backgrounds and Aims

Current research in plant science has concentrated on revealing ontogenetic processes of key attributes in plant evolution. One recently discussed model is the ‘transient model’ successful in explaining some types of inflorescence architectures based on two main principles: the decline of the so called ‘vegetativeness’ (veg) factor and the transient nature of apical meristems in developing inflorescences. This study examines whether both principles find a concrete ontogenetic correlate in inflorescence development.

Methods

To test the ontogenetic base of veg decline and the transient character of apical meristems the ontogeny of meristematic size in developing inflorescences was investigated under scanning electron microscopy. Early and late inflorescence meristems were measured and compared during inflorescence development in 13 eudicot species from 11 families.

Key Results

The initial size of the inflorescence meristem in closed inflorescences correlates with the number of nodes in the mature inflorescence. Conjunct compound inflorescences (panicles) show a constant decrease of meristematic size from early to late inflorescence meristems, while disjunct compound inflorescences present an enlargement by merging from early inflorescence meristems to late inflorescence meristems, implying a qualitative change of the apical meristems during ontogeny.

Conclusions

Partial confirmation was found for the transient model for inflorescence architecture in the ontogeny: the initial size of the apical meristem in closed inflorescences is consistent with the postulated veg decline mechanism regulating the size of the inflorescence. However, the observed biphasic kinetics of the development of the apical meristem in compound racemes offers the primary explanation for their disjunct morphology, contrary to the putative exclusive transient mechanism in lateral axes as expected by the model.     

RFLP analysis of cpDNA in the genus <Emphasis Type="Italic">Hypericum</Emphasis>

The chloroplast DNA of 43 species including 16 sections from the genus Hypericum was studied by PCR-RFLP analysis. The PCR-amplified products of four cpDNA regions, trnC-trnD, psbC-trnS, trnL-trnF and rbcL were digested with four restriction endonucleases. A high level of interspecific variation was detected while intraspecific diversity was not observed. The resulting parsimony analysis indicated the monophyletic assemblage of the sections Androsaemum, Olympia, Drosocarpium and Trigynobrathys. Monophyly of Hypericum is weakly supported, but close relationships of H. perforatum and H. maculatum are indicated. The members of Ascyreia are weakly resolved, but clustering of H. kouytchense and H. oblongifolium is well supported, however, H. reptans is nested with Olympia. CpDNA profiles and the positions on the parsimony tree indicate that the chloroplast donor among the putative parents of the hybrid species H. ×inodorum is H. androsaemum.     

Diversity of inflorescences in the Boutelouinae subtribe (Poaceae: Chloridoideae: Cynodonteae)

The Boutelouinae subtribe is comprised of one monophyletic genus, Bouteloua, with 57 species inhabiting the semi-arid regions of the New World. The inflorescences show significant structural variations, which provides an interesting system to examine their morphological evolution and identify characters and processes that may help to understand the group systematics. The structure of inflorescences was studied in 25 species of Bouteloua. All the species covered under this study have truncated polytelic inflorescences. Structural variations in the inflorescence unit among species may be accounted for by: (1) symmetry of the inflorescence unit, (2) total number of long primary branches, (3) total number of spikelets per branch, (4) number of perfect flowers per spikelet, (5) number of rudimentary flowers, and (6) reproductive system. Homogenization and truncation processes account for the diversity of mature inflorescences that exists in Bouteloua. In this work, we discuss the systematic and taxonomic value of the inflorescence in the Boutelouinae subtribe.     

Variation in scent emission among floral parts and inflorescence developmental stages in beetle-pollinated Protea species (Proteaceae)

Floral fragrances are an important component for pollinator attraction in beetle-pollinated flowers. Several genera in the Proteaceae contain beetle-pollinated species. However, there is no information on the floral scent chemistry of beetle-pollinated members of the family. In this paper we report on the spatial variation and differences between developmental stages in emission of inflorescence (flowerhead) volatiles of four South African Protea species (P. caffra, P. dracomontana, P. simplex, and P. welwitschii) that are pollinated by cetoniine beetles. The scents from different inflorescence parts (bracts, perianth, styles, and nectar) and from successive anthesis stages of whole inflorescences were sampled using dynamic headspace collection and identified using GC–MS. Although the four species shared many scent compounds, possibly reflecting their close phylogenetic relationships and common pollinators, they showed significant differences in overall scent composition due to various species-specific compounds, such as the unique tiglate esters found in the scent of P. welwitschii. The strongest emissions and largest number of volatiles, especially monoterpenes, were from inflorescences at full pollen dehiscence. Senescing inflorescences of two species and nectars of all species emitted proportionally high amounts of acetoin (3-hydroxy-2-butanone) and aromatic alcohols, typical fermentation products. As a consequence, the scent composition of nectar was much more similar among species than was the scent composition of other parts of the inflorescence. These results illustrate how the blends of compounds that make up the overall floral scent are a dynamic consequence of emissions from various plant parts.     

Conservation genetics and geographic patterns of genetic variation of endangered shrub <Emphasis Type="Italic">Ammopiptanthus</Emphasis> (Fabaceae) in northwestern China

Phylogeographic patterns of Ammopiptanthus in northwestern China were examined with internal transcribed spacer (ITS) and three chloroplast intergenic spacers (trnH–psbA, trnL–trnF, and trnS–trnG). Two ITS genotypes (a–b) and 8 chloroplast haplotypes (A–H) were detected. Both ITS genotypes and chloroplast lineages were split in two geographic regions: western Xinjiang and the Alxa Desert. This lineage split was also supported by AMOVA analysis and the Mantel test. AMOVA showed that 89.81 % of variance in Ammopiptanthus occurred between the two geographic regions, and correlation between genetic distances and geographical distances was significant (r = 0.757, p < 0.0001). All populations in western Xinjiang shared haplotype A with high frequency, and range expansion was strongly supported by negative Fu’s F_S value, and mismatch distribution analysis, whereas populations in the Alxa Desert had higher genetic diversity and structure. We speculate that the cold and dry climate during the early Quaternary fragmented habitats of the species, limiting gene flow between regions, and interglacial periods most likely led to the range expansion in western Xinjiang. The low genetic diversity of Ammopiptanthus indicate a significant extinction risk, and protective measures should be taken immediately.     

Inflorescence structure in species of Scleria subgenus Hypoporum and subgenus Scleria (Sclerieae-Cyperaceae)

The objective of this study was to realize a typology approach toward the inflorescences in Scleria in order to provide characters that would have potential use in further taxonomic and phylogenetic research and that would allow identification of the tendencies and processes that could have yielded the variations within Scleria inflorescences. The majority of species studied present a main florescence; Scleria reticularis and S. melanomphala have truncated inflorescences. The variations are related to the grade of development reached by the main florescence and the different parts of the paracladial zone. Major inflorescence variability was found in section Scleria. A change in spikelet sexuality can occur toward the distal parts. There were variations in the distinct species with respect to the hierarchy of the paracladia where the change occurs. Future investigations should center on the ontogenetic aspects of inflorescence development of Scleria, integrating these results, together with those of adult inflorescences, into taxonomic and phylogenetic investigations.     

Phylogenetic relationship of wild and cultivated yam species (Dioscorea spp.) of India inferred from PCR–RFLP analysis of two cpDNA loci

The genus Dioscorea comprises approximately 600 species worldwide and about 50 in India. Dioscorea is economically very useful because of its food and medicinal value. Polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) analysis was employed to study interspecific relationship between four cultivated and thirteen wild species belonging to seven taxonomical sections found in India. Restriction digestion analysis was performed for the amplified products of chloroplast DNA (cpDNA) loci psbA–trnH and trnL-F regions. Out of 17 restriction endonucleases tested, 5 endonucleases had restriction sites in psbA–trnH region and 6 endonucleases had restriction sites in trnL-F region. Digestion of amplified products with these restriction endonucleases showed 70 fragments of which 62 fragments (88 %) were polymorphic. Dendrogram obtained from UPGMA cluster analysis of two combined loci shows D. bulbifera of section Opsophyton to be closely placed with species of sect. Enantiophyllum. High similarity values obtained in this study between D. pentaphylla (sect. Botrysicyos) and D. esculenta (sect. Combilium) support their common origin. The average of genetic similarities between the ten species of Enantiophyllum section was 82.3 % showing their closeness. The present study suggests that the less studied New World species, D. floribunda (sect. Heterostemon) could have evolved from old world section, Lasiophyton. The principal component analysis (PCA) obtained from data of the two loci shows D. deltoidea of sect. Stenophora to be an outgroup. Interspecific genetic similarities showed D. deltoidea with low similarity values ranging from 27.5 to 37.5 % compared with other species and was, therefore, the most divergent species. D. deltoidea of section Stenophora shows distinctness because of its primitive characters. This study, therefore, establishes species relationships between wild and cultivated yams of India which would help in yam crop improvement programmes.     

Parahellenia,a new genus segregated from Hellenia (Costaceae) based on phylogenetic and morphological evidence

Previous studies recognized three major lineages of the family Costaceae: a South American clade, an Asian clade and a Costus clade. However, the genus Hellenia within the Asian clade has been shown to be non-monophyletic and its morphology has not been studied carefully. Therefore, the complete plastid genomes of Hellenia species were obtained and the monophyly of Hellenia was tested through four different datasets in this study. Plastid phylogenomic analyses of Costaceae revealed that Hellenia is strongly supported as paraphyletic. Two major clades are recovered, namely the Hellenia s.s. subclade and the Parahellenia subclade. Phylogenetic analyses based on an enlarged taxon sampling of the Asian clade using a two chloroplast markers dataset (trnK intron and trnL-F spacer) confirmed the paraphyly of Hellenia. Meanwhile, morphological analyses suggested that members of the Parahellenia subclade differ from the remaining Hellenia species in many characters including inflorescences, bracts, stigma, axillary buds, floral tubes and labellum. According to the present molecular and morphological evidence, the latter subclade is recognized as a new genus, Parahellenia. Two new species are described, four new combinations are made, and identification keys are also provided.     

Organ-wise homologies of stipule, leaf and inflorescence between Pisum sativum genetic variants, Delonix regia and Caesalpinia bonduc indicate parallel evolution of morphogenetic regulation

Plants of the garden pea Pisum sativum an annual Papilionaceae species which have a mutation in the COCHLEATA (COCH) gene bear compound stipules of leaf morphology and secondary inflorescences in which flowers are borne in axils of bracteoles on an inflorescence stem. In the wild-type P. sativum stipules are simple foliaceous and flowers are non-bracteolated. Mutants of the coch phenotype are not known in any other plant species. The COCH gene of P. sativum is not yet sequenced. Therefore whether or not the COCH gene is present in species other than P. sativum remains unknown. Based on the principle of parallel evolution, it is thought that there may be leguminous species that possess the coch phenotype. In search of coch species, the Leguminosae flora of Delhi was surveyed for species that demonstrate compound stipules and bracteolated inflorescences. Out of 124 reported in the Leguminosae flora of Delhi, only the perennial Caesalpinioideae tree species Delonix regia and the shrubby vine species Caesalpinia bonduc were observed to have features of the coch mutants of P. sativum. Since the traits of simple foliaceous stipules and bracteoleless secondary inflorescences of wild-type P. sativum are common to many species among more than 19,400 species of family Leguminosae, it is hypothesized that the COCH gene may be as common as the ubiquitously present LEAFY gene (orthologue of UNIFOLIATA gene of P. sativum) in angiosperms.     

Molecular phylogeny of the endemic fern genera Cyrtomidictyum and Cyrtogonellum (Dryopteridaceae) from East Asia

Cyrtomidictyum Ching and Cyrtogonellum Ching are two eastern Asian endemic genera whose taxonomic affinities and phylogenetic relationships have long been controversial. The main uncertainty surrounds the separation of the two genera from the species-rich genus Polystichum. Here we present a phylogenetic study focusing on the phylogenetic relationships of these polystichoid ferns. We reconstructed the relationships based on DNA sequence variation in four chloroplast genome regions, rbcL, atpB, and the intergenic spacers (IGS) rps4-trnS and trnL-trnF. Maximum likelihood and Bayesian inference analyses confirm earlier results that were based on less comprehensive taxon sampling and either only a single gene (rbcL) or two IGS (rps4-trnS and trnL-trnF). Cyrtomidictyum is the sister of the clade of polystichoid ferns that includes Cyrtogonellum, Cyrtomium subser. Balansana and three sections of Polystichum. Cyrtogonellum groups with several species of Polystichum, and constitutes the sister taxon to Polystichum sect. Sphaenopolystichum. We support the recognition of Cyrtomidictyum as circumscribed initially, rather than expansion of the genus to include either several Polystichum species or Cyrtogonellum, some Polystichum and Cyrtomium species. The monophyly of Cyrtomidictyum is supported by morphological characters such as once-pinnate leaves, free venation, prolongated leaf apices, and exindusiate sori. Two synapomorphic indels in the chloroplast genome, one 15-bp deletion in rps4-trnS, and one 3-bp insertion in trnL-trnF further differentiate Cyrtomidictyum from other polystichoid ferns. The close affinity of Cyrtogonellum to section Sphaenopolystichum of Polystichum s.s. is highly supported by molecular data. However, no shared morphological characters or molecular indels have been detected, although the distinctness of Cyrtogonellum is shown by a 13-bp insertion in the rps4-trnS alignment.     

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.Key words: Abrus precatorius, Cicer arietinum, Hardenbergia violacea, Kennedia nigricans, inflorescence, Leguminosae, Papilionoideae, pseudoraceme, Swainsona formosa     

山麦冬及其近缘种DNA条形码研究

通过分析山麦冬及其近缘种cpDNA trnL-F、psbA-trnH间隔区序列特点,探讨trnL-F、psbA-trnH序列作为山麦冬及其近缘种DNA条形码的潜力。分别对两者进行PCR扩增后,并进行纯化测序。其中山麦冬及其近缘种9个物种18个样品的trnL-F序列长度为355~356 bp,在山麦冬属内序列完全一致,但在沿阶草属中存在特异变异位点,可对麦冬与沿阶草两物种进行鉴别。而psbA-trnH序列长度为543~544 bp,仅在麦冬中存在特异鉴别位点。结果表明,trnL-F、psbA-trnH序列由于进化速率低、保守性强,仅适合麦冬类植物属间鉴别的DNA条形码,而在属下水平的应用有一定的局限。     

Molecular systematic study of Cardamine glechomifolia Levl. (Brassicaceae) using internal transcribed spacer sequence of nuclear ribosomal DNA (ITS) and chloroplast trnL and trnL-F sequences

The internal transcribed spacer (ITS) region of nuclear ribosomal DNA, trnL and trnL-F genes of Cardamine glechomifolia Levl. (family Brassicaceae) were sequenced and analyzed with the sequence of related Cardamine species retrieved from NCBI GenBank to detect pattern of evolutionary differentiation. All trees resulting from combined sequence analyses data of ITS, trnL and trnL-F gene resolve that C. glechomifolia – an endemic species to South Korea clade with Cardamine microzyga (100% bootstrap support). The evolutionary history was inferred using the Maximum Parsimony method. The consistency index is (0.588235), the retention index is (0.687500), and the composite index is 0.519622 (0.404412) for all sites and parsimony-informative sites (in parentheses). The result of the analysis using Maximum Parsimony was found congruence with Maximum Likelihood method and in Baseyan analysis.     

What makes a fig: insights from a comparative analysis of inflorescence morphogenesis in Moraceae

Background and AimsMoraceae, the family of mulberry and fig trees, displays small homogeneous flowers but extremely diverse inflorescences ranging from simple and branched to complex and condensed. Inflorescences also vary in flower organization in the receptacle, in the degree of flower condensation and in receptacle shape. Thus, the objective of the present study was to compare the inflorescence morphogenesis of Moraceae species, to investigate whether clades with a similar pollination mode share the same patterns of inflorescence development and the developmental stages at which we observe the key changes resulting in the diversified inflorescence architecture that culminates in the Ficus syconium.MethodsInflorescences at different developmental stages were sampled from Brosimum gaudichaudii, Castilla elastica, Clarisia ilicifolia, Ficus pertusa, Maclura tinctoria and Morus nigra and processed for surface and anatomical analyses.Key ResultsThe inflorescence morphogenesis of the studied species is highly variable. The shape of the inflorescence meristem (bulging, hemispheric or elongated), the initiation order and arrangement of flowers along the receptacle and the occurrence of bracts vary between related species. This diversity originates early during inflorescence development. Brosimum gaudichaudii, C. elastica and F. pertusa have flowers enclosed or immersed within the receptacle, although inflorescences begin their development as flat and open structures, as occurs in the other three study species.ConclusionComparison of the inflorescence morphogenesis in Moraceae species allows us to infer that evolutionary ontogenetic changes driven by pollinators culminate in the enclosure of flowers inside the receptacle, as occurs in the Ficus syconium.     

Phylogeny and infrageneric classification of Correa Andrews (Rutaceae) on the basis of nuclear and chloroplast DNA

This paper presents phylogenies of the small but ecologically and horticulturally important Australian genus Correa (Rutaceae). Consensus phylogenies generated using parsimony were congruent with their counterparts generated by Bayesian analysis, although usually less well resolved. The phylogeny generated from the second internal transcribed spacer region of the nuclear ribosomal DNA supported the monophyly of Correa and identified two well supported clades (one comprising C. lawrenceana and C. baeuerlenii and the other containing all other species of the genus). Phylogenetic reconstructions based on the combined trnL-trnF spacer and the trnK intron (including the matK gene) regions of chloroplast DNA also supported the monophyly of Correa and of the C. lawrenceana/C. baeuerlenii clade, but the topology among the other species differed markedly from that in the ITS-based phylogeny. The major clades identified in the chloroplast phylogenies seemed to follow geographic patterns rather than species boundaries, with different samples of C. glabra bearing chloroplast genotypes from different clades. These patterns are likely to be because of independent evolution of the chloroplast and nuclear genomes, and are typical of cases of introgressive hybridisation among species or incomplete lineage sorting of chloroplast genomes leading to incongruence between chloroplast and nuclear phylogenies. Thus, the phylogenies based on nuclear DNA should reflect species relations better than the chloroplast phylogeny in Correa, and we propose a new subgeneric classification of the genus on the basis of the ITS-based phylogeny and morphology. Correa subgenus Persistens Othman, Duretto and G.J. Jord., containing C. lawrenceana and C. baeuerlenii, is formally described.     

Floral display size in comfrey, Symphytum officinale L. (Boraginaceae): relationships with visitation by three bumblebee species and subsequent seed set

The fecundity of insect-pollinated plants may not be linearly related to the number of flowers produced, since floral display will influence pollinator foraging patterns. We may expect more visits to plants with more flowers, but do these large plants receive more or fewer visits per flower than small plants? Do all pollinator species respond in the same way? We would also expect foragers to move less between plants when the number of flowers per plant are large, which may reduce cross-pollination compared to plants with few flowers. We examine the relationships between numbers of inflorescence per plant, bumblebee foraging behaviour and seed set in comfrey, Symphytum officinale, a self-incompatible perennial herb. Bumblebee species differed in their response to the size of floral display. More individuals of Bombus pratorum and the nectar-robbing B.?terrestris were attracted to plants with larger floral displays, but B. pascuorum exhibited no increase in recruitment according to display size. Once attracted, all bee species visited more inflorescences per plant on plants with more inflorescences. Overall the visitation rate per inflorescence and seed set per flower was independent of the number of inflorescences per plant. Variation in seed set was not explained by the numbers of bumblebees attracted or by the number of inflorescences they visited for any bee species. However, the mean seed set per flower (1.18) was far below the maximum possible (4 per flower). We suggest that in this system seed set is not limited by pollination but by other factors, possibly nutritional resources.     

Metamerism,heterochrony, and inflorescence morphology of the Pithecellobium-complex (Leguminosae: Mimosoideae: Ingeae)

The diverse inflorescence morphology of species in the Pithecellobium-complex is shown to be a result of: 1) the organization of the components of the inflorescence and their relative positions; 2) the hierarchical relationship of the axes of the inflorescences and the position they assume in total tree architecture; and 3) heterochronic development of the components of the inflorescence. It is shown that the typological system of nomenclature of inflorescences leads to false assumptions of homology and therefore must be discarded. The morphology of inflorescences is discussed in terms of metamerism, and the term Repeating Growth Unit (RGU) is introduced and is defined as the smallest complete sequence of metamers produced by a meristem. A module is defined as the sequence of RGUs produced by a meristem. An inflorescence is defined as that sequence of metamers in an RGU which participates in the production and/or presentation of flowers and fruit. Heterochrony, proleptic and sylleptic buds, and shoot dimorphism are discussed and their role in modifying inflorescence morphology in the Pithecellobium-complex is illustrated. Examples from the Pithecellobium-complex are provided which demonstrate the various modifications of the inflorescence that result from the interaction of these various phenomena.     

Organographic and ontogenetic studies on the inflorescence ofLespedeza cuneata (Dum.-Cours.) G. Don (Leguminosae)

Structure of inflorescence and its variation were organographically and ontogenetically studied inLespedeza cuneata (Dum.-Cours.) G. Don. An axillary inflorescence of the species forms a compound inflorescence which is composed of three or four component inflorescences. Each component inflorescence bears four (rarely six), three, two, or one flowers. Based on the arrangement of inflorescence phyllomes, the component inflorescence with four flowers is interpreted as a pseudoraceme bearing two shortened lateral shoots (partial inflorescences) each of which has two flowers. The component inflorescence with one flower appears to be terminated by the flower and to compose the cyme. Organographic observations revealed that the terminally located flower is not truly terminal, but axillary in origin. Ontogenetic observations showed that the apices of component inflorescence and partial inflorescence exist in early developmental stages in spite of variation in the form of component inflorescence. The terminally located flower in the cyme-like inflorescence was thus demonstrated to be laterally borne on the partial inflorescence axis. The component inflorescence composing the cyme-like one inL. cuneata is a reduced form in the number of partial inflorescences and of flowers from the pseudoraceme. The cyme-like inflorescence inL. cuneata resembles the inflorescence ofKummerowia.