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1.  Resurrection of the genus Staphisagria J. Hill, sister to all the other Delphinieae (Ranunculaceae)  
PhytoKeys  2011;21-26.
Molecular sequence data show that the three species oDelphinium subg. Staphisagria (J. Hill) Peterm. form the sister clade to Aconitum L., Aconitella SpachConsolida (DC.) S.F. Gray, and all remaining species of Delphinium L. To account for this finding we resurrect Staphisagria J. Hill (1756). Names in Staphisagria are available for two of the species. We here make the required new combination for the third species, Staphisagria picta (Willd.) F. Jabbour, provide a key to the species, and illustrate one of them.
doi:10.3897/phytokeys.7.2010
PMCID: PMC3261041  PMID: 22287922
Aconitum; Delphinium; Mediterranean region; molecular phylogeny; nomenclature; Staphisagria
2.  Evolutionary Trends in the Flowers of Asteridae: Is Polyandry an Alternative to Zygomorphy? 
Annals of Botany  2008;102(2):153-165.
Background and Aims
Floral symmetry presents two main states in angiosperms, actinomorphy (polysymmetry or radial symmetry) and zygomorphy (monosymmetry or bilateral symmetry). Transitions from actinomorphy to zygomorphy have occurred repeatedly among flowering plants, possibly in coadaptation with specialized pollinators. In this paper, the rules controlling the evolution of floral symmetry were investigated to determine in which architectural context zygomorphy can evolve.
Methods
Floral traits potentially associated with perianth symmetry shifts in Asteridae, one of the major clades of the core eudicots, were selected: namely the perianth merism, the presence and number of spurs, and the androecium organ number. The evolution of these characters was optimized on a composite tree. Correlations between symmetry and the other morphological traits were then examined using a phylogenetic comparative method.
Key Results
The analyses reveal that the evolution of floral symmetry in Asteridae is conditioned by both androecium organ number and perianth merism and that zygomorphy is a prerequisite to the emergence of spurs.
Conclusions
The statistically significant correlation between perianth zygomorphy and oligandry suggests that the evolution of floral symmetry could be canalized by developmental or spatial constraint. Interestingly, the evolution of polyandry in an actinomorphic context appears as an alternative evolutionary pathway to zygomorphy in Asteridae. These results may be interpreted either in terms of plant–pollinator adaptation or in terms of developmental or physical constraints. The results are discussed in relation to current knowledge about the molecular bases underlying floral symmetry.
doi:10.1093/aob/mcn082
PMCID: PMC2712368  PMID: 18511411
Floral symmetry; architectural constraints; Asteridae; comparative analysis; composite tree; correlated evolution; evolutionary scenario
3.  Ovule Morphogenesis in Ranunculaceae and its Systematic Significance 
Annals of Botany  2007;101(3):447-462.
Background and Aims
Ranunculaceae has a prominent phylogenetic position in Ranunculales which appears at the base of eudicots. The aims of the present paper are to reveal the features of ovule morphogenesis in different taxa and gain a better understanding of the systematics of Ranunculaceae.
Methods
Flowers of 17 species from three subfamilies, nine tribes and 16 genera of Ranunculaceae, at successive developmental stages, were collected in the wild and studied with a scanning electron microscope.
Key Results
The integuments in the unitegmic ovules in Helleborus, Ranunculus and Oxygraphis, as well as the inner integuments in the bitegmic genera, initiate annularly and eventually become cup-shaped. However, the integuments in the unitegmic ovules in Anemone and Clematis, as well as the outer integuments in the bitegmic genera, arise semi-annularly and eventually become hood-shaped. Different kinds of appendages appear on the ovules during development. In Coptis of subfamily Coptidoideae, a wrap-shaped appendage arises outside the ovule and envelopes the ovule entirely. In the genera of subfamily Thalictroideae and tribe Anemoneae of subfamily Ranunculoideae, appendages appear on the placenta, the funicle or both. In tribe Helleboreae of subfamily Ranunculoideae, an alary appendage is initiated where the integument and the funicle join and becomes hood-shaped.
Conclusions
Ovule morphogenesis characteristics are significant in classification at the levels of subfamilies and tribes. The initiation patterns of the integuments and the development of appendages show diversity in Ranunculaceae. The present observations suggest that the bitegmic, hood-shaped outer integument and endostomic micropyle are primitive while the unitegmic, cupular-shaped outer integument and bistomic micropyle are derivative.
doi:10.1093/aob/mcm298
PMCID: PMC2701822  PMID: 18065776
Ranunculaceae; ovule; morphogenesis; systematics
4.  Virus-induced gene silencing (VIGS) in Cysticapnos vesicaria, a zygomorphic-flowered Papaveraceae (Ranunculales, basal eudicots) 
Annals of Botany  2012;109(5):911-920.
Background and Aims
Studies of evolutionary diversification in the basal eudicot family Papaveraceae, such as the transition from actinomorphy to zygomorphy, are hampered by the lack of comparative functional studies. So far, gene silencing methods are only available in the actinomorphic species Eschscholzia californica and Papaver somniferum. This study addresses the amenability of Cysticapnos vesicaria, a derived fumitory with zygomorphic flowers, to virus-induced gene silencing (VIGS), and describes vegetative and reproductive traits in this species.
Methods
VIGS-mediated downregulation of the C. vesicaria PHYTOENE DESATURASE gene (CvPDS) and of the FLORICAULA gene CvFLO was carried out using Agrobacterium tumefaciens transfer of Tobacco rattle virus (TRV)-based vectors. Wild-type and vector-treated plants were characterized using reverse transcription–PCR (RT–PCR), in situ hybridization, and macroscopic and scanning electron microscopic imaging.
Key Results
Cysticapnos vesicaria germinates rapidly, can be grown at high density, has a short life cycle and is self-compatible. Inoculation of C. vesicaria with a CvPDS-VIGS vector resulted in strong photobleaching of green parts and reduction of endogenous CvPDS transcript levels. Gene silencing persisted during inflorescence development until fruit set. Inoculation of plants with CvFLO-VIGS affected floral phyllotaxis, symmetry and floral organ identities.
Conclusions
The high penetrance, severity and stability of pTRV-mediated silencing, including the induction of meristem-related phenotypes, make C. vesicaria a very promising new focus species for evolutionary–developmental (evo–devo) studies in the Papaveraceae. This now enables comparative studies of flower symmetry, inflorescence determinacy and other traits that diversified in the Papaveraceae.
doi:10.1093/aob/mcs008
PMCID: PMC3310490  PMID: 22307568
Agrobacterium tumefaciens; basal eudicots; Cysticapnos vesicaria; FLORICAULA; Papaveraceae; PHYTOENE DESATURASE; Ranunculales; Tobacco rattle virus; VIGS, zygomorphy
5.  Expressions of ECE-CYC2 clade genes relating to abortion of both dorsal and ventral stamens in Opithandra (Gesneriaceae) 
Background
ECE-CYC2 clade genes known in patterning floral dorsoventral asymmetry (zygomorphy) in Antirrhinum majus are conserved in the dorsal identity function including arresting the dorsal stamen. However, it remains uncertain whether the same mechanism underlies abortion of the ventral stamens, an important morphological trait related to evolution and diversification of zygomorphy in Lamiales sensu lato, a major clade of predominantly zygomorphically flowered angiosperms. Opithandra (Gesneriaceae) is of particular interests in addressing this question as it is in the base of Lamiales s.l., an early representative of this type zygomorphy.
Results
We investigated the expression patterns of four ECE-CYC2 clade genes and two putative target cyclinD3 genes in Opithandra using RNA in situ hybridization and RT-PCR. OpdCYC gene expressions were correlated with abortion of both dorsal and ventral stamens in Opithandra, strengthened by the negatively correlated expression of their putative target OpdcyclinD3 genes. The complement of OpdcyclinD3 to OpdCYC expressions further indicated that OpdCYC expressions were related to the dorsal and ventral stamen abortion through negative effects on OpdcyclinD3 genes.
Conclusion
These results suggest that ECE-CYC2 clade TCP genes are not only functionally conserved in the dorsal stamen repression, but also involved in arresting ventral stamens, a genetic mechanism underlying the establishment of zygomorphy with abortion of both the dorsal and ventral stamens evolved in angiosperms, especially within Lamiales s.l.
doi:10.1186/1471-2148-9-244
PMCID: PMC2763874  PMID: 19811633
6.  High time for a roll call: gene duplication and phylogenetic relationships of TCP-like genes in monocots 
Annals of Botany  2011;107(9):1533-1544.
Background and Aims
The TCP family is an ancient group of plant developmental transcription factors that regulate cell division in vegetative and reproductive structures and are essential in the establishment of flower zygomorphy. In-depth research on eudicot TCPs has documented their evolutionary and developmental role. This has not happened to the same extent in monocots, although zygomorphy has been critical for the diversification of Orchidaceae and Poaceae, the largest families of this group. Investigating the evolution and function of TCP-like genes in a wider group of monocots requires a detailed phylogenetic analysis of all available sequence information and a system that facilitates comparing genetic and functional information.
Methods
The phylogenetic relationships of TCP-like genes in monocots were investigated by analysing sequences from the genomes of Zea mays, Brachypodium distachyon, Oryza sativa and Sorghum bicolor, as well as EST data from several other monocot species.
Key Results
All available monocot TCP-like sequences are associated in 20 major groups with an average identity ≥64 % and most correspond to well-supported clades of the phylogeny. Their sequence motifs and relationships of orthology were documented and it was found that 67 % of the TCP-like genes of Sorghum, Oryza, Zea and Brachypodium are in microsyntenic regions. This analysis suggests that two rounds of whole genome duplication drove the expansion of TCP-like genes in these species.
Conclusions
A system of classification is proposed where putative or recognized monocot TCP-like genes are assigned to a specific clade of PCF-, CIN- or CYC/tb1-like genes. Specific biases in sequence data of this family that must be tackled when studying its molecular evolution and phylogeny are documented. Finally, the significant retention of duplicated TCP genes from Zea mays is considered in the context of balanced gene drive.
doi:10.1093/aob/mcr059
PMCID: PMC3108806  PMID: 21444336
TCP; tb1; CYCLOIDEA; PCF1; Zea mays; Oryza sativa; Brachypodium distachyon; Sorghum bicolor; gene family; monocot; whole genome duplication
7.  The effect of flower position on variation and covariation in floral traits in a wild hermaphrodite plant 
BMC Plant Biology  2010;10:91.
Background
Floral traits within plants can vary with flower position or flowering time. Within an inflorescence, sexual allocation of early produced basal flowers is often female-biased while later produced distal flowers are male-biased. Such temporal adjustment of floral resource has been considered one of the potential advantages of modularity (regarding a flower as a module) in hermaphrodites. However, flowers are under constraints of independent evolution of a given trait. To understand flower diversification within inflorescences, here we examine variation and covariation in floral traits within racemes at the individual and the maternal family level respectively in an alpine herb Aconitum gymnandrum (Ranunculaceae).
Results
We found that floral traits varied significantly with flower position and among families, and position effects were family-specific. Most of the variance of floral traits was among individuals rather than among flowers within individuals or among families. Significant phenotypic correlations between traits were not affected by position, indicating trait integration under shared developmental regulation. In contrast, positive family-mean correlations in floral traits declined gradually from basal to distal flowers (nine significant correlations among floral traits in basal flowers and only three in distal flowers), showing position-specificity. Therefore, the pattern and magnitude of genetic correlations decreased with flower position.
Conclusions
This finding on covariation pattern in floral reproductive structures within racemes has not been revealed before, providing insights into temporal variation and position effects in floral traits within plants and the potential advantages of modularity in hermaphrodites.
doi:10.1186/1471-2229-10-91
PMCID: PMC3095358  PMID: 20482889
8.  Environmental and molecular analysis of the floral transition in the lower eudicot Aquilegia formosa 
EvoDevo  2011;2:4.
Background
Flowering is a critical transition in plant development, the timing of which can have considerable fitness consequences. Until recently, research into the genetic control of flowering time and its associated developmental changes was focused on core eudicots (for example, Arabidopsis) or monocots (for example, Oryza). Here we examine the flowering response of Aquilegia formosa, a member of the eudicot order Ranunculales that is emerging as an important model for the investigation of plant ecology and evolution.
Results
We have determined that A. formosa has a strong vernalization requirement but little or no photoperiod response, making it a day neutral (DN) plant. Consistent with this, the Aquilegia homolog of FLOWERING LOCUS T (AqFT) is expressed in both long and short days but surprisingly, the locus is expressed before the transition to flowering. In situ hybridizations with homologs of several Arabidopsis Floral Pathway Integrators (FPIs) do not suggest conserved functions relative to Arabidopsis, the potential exceptions being AqLFY and AqAGL24.2.
Conclusions
In Aquilegia, vernalization is critical to flowering but this signal is not strictly required for the transcriptional activation of AqFT. The expression patterns of AqLFY and AqAGL24.2 suggest a hypothesis for the development of Aquilegia's determinate inflorescence whereby their differential expression controls the progression of each meristem from inflorescence to floral identity. Interestingly, none of the Aquilegia expression patterns are consistent with a function in floral repression which, combined with the lack of a FLC homolog, means that new candidate genes must be identified for the control of vernalization response in Aquilegia.
doi:10.1186/2041-9139-2-4
PMCID: PMC3049749  PMID: 21329499
9.  Virus-induced gene silencing as a tool for functional analyses in the emerging model plant Aquilegia (columbine, Ranunculaceae) 
Plant Methods  2007;3:6.
Background
The lower eudicot genus Aquilegia, commonly known as columbine, is currently the subject of extensive genetic and genomic research aimed at developing this taxon as a new model for the study of ecology and evolution. The ability to perform functional genetic analyses is a critical component of this development process and ultimately has the potential to provide insight into the genetic basis for the evolution of a wide array of traits that differentiate flowering plants. Aquilegia is of particular interest due to both its recent evolutionary history, which involves a rapid adaptive radiation, and its intermediate phylogenetic position between core eudicot (e.g., Arabidopsis) and grass (e.g., Oryza) model species.
Results
Here we demonstrate the effective use of a reverse genetic technique, virus-induced gene silencing (VIGS), to study gene function in this emerging model plant. Using Agrobacterium mediated transfer of tobacco rattle virus (TRV) based vectors, we induce silencing of PHYTOENE DESATURASE (AqPDS) in Aquilegia vulgaris seedlings, and ANTHOCYANIDIN SYNTHASE (AqANS) and the B-class floral organ identity gene PISTILLATA in A. vulgaris flowers. For all of these genes, silencing phenotypes are associated with consistent reduction in endogenous transcript levels. In addition, we show that silencing of AqANS has no effect on overall floral morphology and is therefore a suitable marker for the identification of silenced flowers in dual-locus silencing experiments.
Conclusion
Our results show that TRV-VIGS in Aquilegia vulgaris allows data to be rapidly obtained and can be reproduced with effective survival and silencing rates. Furthermore, this method can successfully be used to evaluate the function of early-acting developmental genes. In the future, data derived from VIGS analyses will be combined with large-scale sequencing and microarray experiments already underway in order to address both recent and ancient evolutionary questions.
doi:10.1186/1746-4811-3-6
PMCID: PMC1855323  PMID: 17430595
10.  Similar Genetic Mechanisms Underlie the Parallel Evolution of Floral Phenotypes 
PLoS ONE  2012;7(4):e36033.
The repeated origin of similar phenotypes is invaluable for studying the underlying genetics of adaptive traits; molecular evidence, however, is lacking for most examples of such similarity. The floral morphology of neotropical Malpighiaceae is distinctive and highly conserved, especially with regard to symmetry, and is thought to result from specialization on oil-bee pollinators. We recently demonstrated that CYCLOIDEA2–like genes (CYC2A and CYC2B) are associated with the development of the stereotypical floral zygomorphy that is critical to this plant–pollinator mutualism. Here, we build on this developmental framework to characterize floral symmetry in three clades of Malpighiaceae that have independently lost their oil bee association and experienced parallel shifts in their floral morphology, especially in regard to symmetry. We show that in each case these species exhibit a loss of CYC2B function, and a strikingly similar shift in the expression of CYC2A that is coincident with their shift in floral symmetry. These results indicate that similar floral phenotypes in this large angiosperm clade have evolved via parallel genetic changes from an otherwise highly conserved developmental program.
doi:10.1371/journal.pone.0036033
PMCID: PMC3338646  PMID: 22558314
11.  Divergent genetic mechanisms underlie reversals to radial floral symmetry from diverse zygomorphic flowered ancestors 
Malpighiaceae possess flowers with a unique bilateral symmetry (zygomorphy), which is a hypothesized adaptation associated with specialization on neotropical oil bee pollinators. Gene expression of two representatives of the CYC2 lineage of floral symmetry TCP genes, CYC2A and CYC2B, demarcate the adaxial (dorsal) region of the flower in the characteristic zygomorphic flowers of most Malpighiaceae. Several clades within the family, however, have independently lost their specialized oil bee pollinators and reverted to radial flowers (actinomorphy) like their ancestors. Here, we investigate CYC2 expression associated with four independent reversals to actinomorphy. We demonstrate that these reversals are always associated with alteration of the highly conserved CYC2 expression pattern observed in most New World (NW) Malpighiaceae. In NW Lasiocarpus and Old World (OW) Microsteria, the expression of CYC2-like genes has expanded to include the ventral region of the corolla. Thus, the pattern of gene expression in these species has become radialized, which is comparable to what has been reported in the radial flowered legume clade Cadia. In striking contrast, in NW Psychopterys and OW Sphedamnocarpus, CYC2-like expression is entirely absent or at barely detectable levels. This is more similar to the pattern of CYC2 expression observed in radial flowered Arabidopsis. These results collectively indicate that, regardless of geographic distribution, reversals to similar floral phenotypes in this large tropical angiosperm clade have evolved via different genetic changes from an otherwise highly conserved developmental program.
doi:10.3389/fpls.2013.00302
PMCID: PMC3747361  PMID: 23970887
CYC2-like genes; development; floral symmetry; Malpighiaceae; reversals
12.  Intra-plant Variation in Nectar Sugar Composition in Two Aquilegia Species (Ranunculaceae): Contrasting Patterns under Field and Glasshouse Conditions 
Annals of Botany  2007;99(4):653-660.
Background and Aims
Intra-specific variation in nectar chemistry under natural conditions has been only rarely explored, yet it is an essential aspect of our understanding of how pollinator-mediated selection might act on nectar traits. This paper examines intra-specific variation in nectar sugar composition in field and glasshouse plants of the bumblebee-pollinated perennial herbs Aquilegia vulgaris subsp. vulgaris and Aquilegia pyrenaica subsp. cazorlensis (Ranunculaceae). The aims of the study are to assess the generality of extreme intra-plant variation in nectar sugar composition recently reported for other species in the field, and gaining insight on the possible mechanisms involved.
Methods
The proportions of glucose, fructose and sucrose in single-nectary nectar samples collected from field and glasshouse plants were determined using high performance liquid chromatography. A hierarchical variance partition was used to dissect total variance into components due to variation among plants, flowers within plants, and nectaries within flowers.
Key Results
Nectar of the two species was mostly sucrose-dominated, but composition varied widely in the field, ranging from sucrose-only to fructose-dominated. Most intra-specific variance was due to differences among nectaries of the same flower, and flowers of the same plant. The high intra-plant variation in sugar composition exhibited by field plants vanished in the glasshouse, where nectar composition emerged as a remarkably constant feature across plants, flowers and nectaries.
Conclusions
In addition to corroborating the results of previous studies documenting extreme intra-plant variation in nectar sugar composition in the field, this study suggests that such variation may ultimately be caused by biotic factors operating on the nectar in the field but not in the glasshouse. Pollinator visitation and pollinator-borne yeasts are suggested as likely causal agents.
doi:10.1093/aob/mcl291
PMCID: PMC2802931  PMID: 17259227
Abiotic environment; Aquilegia pyrenaica subsp. cazorlensis; Aquilegia vulgaris subsp. vulgaris; biotic factors; field conditions; glasshouse; Iberian Peninsula; inter- and intra-specific variation; nectar-sugar composition; nectary; variance components
13.  Genetic Analysis of Floral Symmetry in Van Gogh's Sunflowers Reveals Independent Recruitment of CYCLOIDEA Genes in the Asteraceae 
PLoS Genetics  2012;8(3):e1002628.
The genetic basis of floral symmetry is a topic of great interest because of its effect on pollinator behavior and, consequently, plant diversification. The Asteraceae, which is the largest family of flowering plants, is an ideal system in which to study this trait, as many species within the family exhibit a compound inflorescence containing both bilaterally symmetric (i.e., zygomorphic) and radially symmetric (i.e., actinomorphic) florets. In sunflower and related species, the inflorescence is composed of a single whorl of ray florets surrounding multiple whorls of disc florets. We show that in double-flowered (dbl) sunflower mutants (in which disc florets develop bilateral symmetry), such as those captured by Vincent van Gogh in his famous nineteenth-century sunflower paintings, an insertion into the promoter region of a CYCLOIDEA (CYC)-like gene (HaCYC2c) that is normally expressed specifically in WT rays is instead expressed throughout the inflorescence, presumably resulting in the observed loss of actinomorphy. This same gene is mutated in two independent tubular-rayed (tub) mutants, though these mutations involve apparently recent transposon insertions, resulting in little or no expression and radialization of the normally zygomorphic ray florets. Interestingly, a phylogenetic analysis of CYC-like genes from across the family suggests that different paralogs of this fascinating gene family have been independently recruited to specify zygomorphy in different species within the Asteraceae.
Author Summary
The evolution of flower shape and symmetry is of great interest to plant biologists, because it can affect pollinator behavior. Species in the flowering plant family Asteraceae exhibit flower heads that can contain both bilaterally and radially symmetric flowers. In this study, we identify a CYCLOIDEA-like gene that is responsible for determining flower symmetry in sunflower. Mis-expression of this gene causes a double-flowered phenotype, similar to those captured in Vincent van Gogh's famous nineteenth-century paintings, whereas loss of gene function causes radialization of the normally bilaterally symmetric ray florets. Interestingly, this gene is not orthologous to the CYCLOIDEA-like gene responsible for floral symmetry in other members of the Asteraceae, providing evidence of the parallel recruitment of different members of the same gene family for the same function.
doi:10.1371/journal.pgen.1002628
PMCID: PMC3315478  PMID: 22479210
14.  Evolution of Perianth and Stamen Characteristics with Respect to Floral Symmetry in Ranunculales 
Annals of Botany  2007;100(3):631-640.
Background and Aims
Floral symmetry presents two main states in angiosperms, namely polysymmetry and monosymmetry. Monosymmetry is thought to have evolved several times independently from polysymmetry, possibly in co-adaptation with specialized pollinators. Monosymmetry commonly refers to the perianth, even though associated androecium modifications have been reported. The evolution of perianth symmetry is examined with respect to traits of flower architecture in the Ranunculales, the sister group to all other eudicots, which present a large diversity of floral forms.
Methods
Characters considered were perianth merism, calyx, corolla and androecium symmetry, number of stamens and spurs. Character evolution was optimized on a composite phylogenetic tree of Ranunculales using maximum parsimony.
Key Results
The ancestral state for merism could not be inferred because the basalmost Eupteleaceae lack a perianth and have a variable number of stamens. The Papaveraceae are dimerous, and the five other families share a common trimerous ancestor. Shifts from trimery to dimery (or reverse) are observed. Pentamery evolved in Ranunculaceae. Ranunculales except Eupteleaceae, present a polysymmetric ancestral state. Monosymmetry evolved once within Papaveraceae, Ranunculaceae and Menispermaceae (female flowers only). Oligandry is the ancestral state for all Ranunculales, and polyandry evolved several times independently, in Papaveraceae, Menispermaceae, Berberidaceae and Ranunculaceae, with two reversions to oligandry in the latter. The ancestral state for androecium symmetry is ambiguous for the Ranunculales, while polysymmetry evolved immediately after the divergence of Eupteleaceae. A disymmetric androecium evolved in Papaveraceae. The ancestral state for spurs is none. Multiple spurs evolved in Papaveraceae, Berberidaceae and Ranunculaceae, and single spurs occur in Papaveraceae and Ranunculaceae.
Conclusions
The evolution of symmetry appears disconnected from changes in merism and stamen number, although monosymmetry never evolved in the context of an open ground plan. In bisexual species, monosymmetry evolved coincidently with single spurs, allowing us to propose an evolutionary scenario for Papaveraceae.
doi:10.1093/aob/mcm041
PMCID: PMC2533616  PMID: 17428835
Floral symmetry; Ranunculales; perianth; androecium; stamen; spur; merism; evo-devo
15.  On ‘various contrivances’: pollination, phylogeny and flower form in the Solanaceae 
Members of the euasterid angiosperm family Solanaceae have been characterized as remarkably diverse in terms of flower morphology and pollinator type. In order to test the relative contribution of phylogeny to the pattern of distribution of floral characters related to pollination, flower form and pollinators have been mapped onto a molecular phylogeny of the family. Bilateral flower symmetry (zygomorphy) is prevalent in the basal grades of the family, and more derived clades have flowers that are largely radially symmetric, with some parallel evolution of floral bilateralism. Pollinator types (‘syndromes’) are extremely homoplastic in the family, but members of subfamily Solanoideae are exceptional in being largely bee pollinated. Pollinator relationships in those genera where they have been investigated more fully are not as specific as flower morphology and the classical pollinator syndrome models might suggest, and more detailed studies in some particularly variable genera, such as Iochroma and Nicotiana, are key to understanding the role of pollinators in floral evolution and adaptive radiation in the family. More studies of pollinators in the field are a priority.
doi:10.1098/rstb.2009.0236
PMCID: PMC2838263  PMID: 20047871
adaptive radiation; flower morphology; phylogeny; Solanaceae; pollination syndrome; homoplasy
16.  Parallel evolution of TCP and B-class genes in Commelinaceae flower bilateral symmetry 
EvoDevo  2012;3:6.
Background
Flower bilateral symmetry (zygomorphy) has evolved multiple times independently across angiosperms and is correlated with increased pollinator specialization and speciation rates. Functional and expression analyses in distantly related core eudicots and monocots implicate independent recruitment of class II TCP genes in the evolution of flower bilateral symmetry. Furthermore, available evidence suggests that monocot flower bilateral symmetry might also have evolved through changes in B-class homeotic MADS-box gene function.
Methods
In order to test the non-exclusive hypotheses that changes in TCP and B-class gene developmental function underlie flower symmetry evolution in the monocot family Commelinaceae, we compared expression patterns of teosinte branched1 (TB1)-like, DEFICIENS (DEF)-like, and GLOBOSA (GLO)-like genes in morphologically distinct bilaterally symmetrical flowers of Commelina communis and Commelina dianthifolia, and radially symmetrical flowers of Tradescantia pallida.
Results
Expression data demonstrate that TB1-like genes are asymmetrically expressed in tepals of bilaterally symmetrical Commelina, but not radially symmetrical Tradescantia, flowers. Furthermore, DEF-like genes are expressed in showy inner tepals, staminodes and stamens of all three species, but not in the distinct outer tepal-like ventral inner tepals of C. communis.
Conclusions
Together with other studies, these data suggest parallel recruitment of TB1-like genes in the independent evolution of flower bilateral symmetry at early stages of Commelina flower development, and the later stage homeotic transformation of C. communis inner tepals into outer tepals through the loss of DEF-like gene expression.
doi:10.1186/2041-9139-3-6
PMCID: PMC3359255  PMID: 22394484
B class genes; Commelinaceae; CYCLOIDEA; homeotic change; monocots; tepals; teosinte branched1
17.  Presence of yeasts in floral nectar is consistent with the hypothesis of microbial-mediated signaling in plant-pollinator interactions 
Plant Signaling & Behavior  2009;4(11):1102-1104.
Olfactory floral signals are significant factors in plant-pollinator mutualisms. Recently, unusual fermentation odors have been described in the nectar and flowers of some species. Since yeasts are common inhabitants of many angiosperms nectars, this raises the possibility that nectar yeasts may act as causal agents of fermentation odors in flowers and, therefore, as possible intermediate agents in plant signaling to pollinators. A recent field study has reported that nectar yeasts were quite frequent in floral nectar across three different regions in Europe and America, where they reached high densities (up to 105 cells/mm3). Yeast incidence in floral nectar differed widely across plant host species in all sampling sites. A detailed study currently in progress on one of the species surveyed in that study (Helleborus foetidus, Ranunculaceae) has detected that, in addition to interespecific differences in yeast incidence, there is also a strong component of variance in yeast abundance that takes place at the subindividual level (among flowers of the same plant, among nectaries of the same flower). If yeast metabolism is eventually proved to contribute significantly to floral scent, then multilevel patchiness in the distribution of nectar yeasts (among species, among individuals within species, and among flowers and nectaries of the same individual) might contribute to concomitant multilevel variation in plant signaling and, eventually, also in pollination success, pollen flow and plant fitness.
PMCID: PMC2819527  PMID: 20009562
nectar; yeast; scent; plant-animal interaction; plant signaling
18.  Floral isolation between Aquilegia formosa and Aquilegia pubescens 
The acquisition of floral nectar spurs is correlated with increased species diversity across multiple clades. We tested whether variation in nectar spurs influences reproductive isolation and, thus, can potentially promote species diversity using two species of Aquilegia, Aquilegia formosa and Aquilegia pubescens, which form narrow hybrid zones. Floral visitors strongly discriminated between the two species both in natural populations and at mixed-species arrays of individual flowers. Bees and hummingbirds visited flowers of A. formosa at a much greater rate than flowers of A. pubescens. Hawkmoths, however, nearly exclusively visited flowers of A. pubescens. We found that altering the orientation of A. pubescens flowers from upright to pendent, like the flowers of A. formosa, reduced hawkmoth visitation by an order of magnitude. In contrast, shortening the length of the nectar spurs of A. pubescens flowers to a length similar to A. formosa flowers did not affect hawkmoth visitation. However, pollen removal was significantly reduced in flowers with shortened nectar spurs. These data indicate that floral traits promote floral isolation between these species and that specific floral traits affect floral isolation via ethological isolation while others affect floral isolation via mechanical isolation.
doi:10.1098/rspb.1999.0915
PMCID: PMC1690454
19.  Cyperus rotundus, a substitute for Aconitum heterophyllum: Studies on the Ayurvedic concept of Abhava Pratinidhi Dravya (drug substitution) 
In the absence of a desired first choice medicinal herb, classical Ayurveda recommends use of a functionally similar substitute. Post 16th century Ayurvedic texts and lexicons give specific examples of possible substitutes. Here we report a preliminary study of one such Ayurvedic substitution pair: Musta (Cyperus rotundus L., Cyperaceae), a common weed, for the rare Himalayan species, Ativisha (Aconitum heterophyllum Wall. ex Royle; Ranunculaceae). The study's strategy was to use modern phytochemical and pharmacological methods to test the two herbs for biochemical and metabolic similarities and differences, and literary studies to compare their Ayurvedic properties, a novel trans-disciplinary approach. No previous scientific paper has compared the two herbs’ bioactivities or chemical profiles. Despite being taxonomically unrelated, the first choice, but relatively unavailable (Abhava) plant, A. heterophyllum, and its substitute (Pratinidhi) C. rotundus, are not only similar in Ayurvedic pharmacology (Dravyaguna) profile, but also in phytochemical and anti-diarrheal properties. These observations indicate that Ayurveda may attach more importance to pharmacological properties of raw drugs than to their botanical classification. Further research into the nature of raw drugs named could open up new areas of medicinal plant classification, linking chemistry and bioactivity. Understanding the logic behind the Ayurvedic concept of Abhava Pratinidhi Dravya (drug substitution) could lead to new methods of identifying legitimate drug alternatives, and help solve industry's problems of crude drug shortage.
doi:10.4103/0975-9476.59825
PMCID: PMC3149390  PMID: 21829299
Abhava Pratinidhi Dravya; Ayurveda; anti-diarrheal; drug substitution
20.  Phylogenetic position and taxonomy of the enigmatic Orobanche krylowii (Orobanchaceae), a predominatly Asian species newly found in Albania (SE Europe) 
Phytotaxa  2013;137(1):1-14.
We report on the occurrence of Orobanche krylowii in the Alpet Shqiptare (Prokletije, Albanian Alps) mountain range in northern Albania (Balkan Peninsula). The species was previously known only from eastern-most Europe (Volga-Kama River in Russia), more than 2500 km away, and from adjacent Siberia and Central Asia. We used morphological evidence as well as nuclear ribosomal ITS sequences to show that the Albanian population indeed belongs to O. krylowii and that its closest relative is the European O. lycoctoni, but not O. elatior as assumed in the past. Both Orobanche krylowii and O. lycoctoni parasitize Ranunculaceae (Thalictrum spp. and Aconitum lycoctonum, respectively). We provide an identification key and a taxonomic treatment for O. krylowii, and suggest the IUCN category CE (critically endangered) for the highly disjunct Albanian population.
doi:10.11646/phytotaxa.137.1.1
PMCID: PMC3868937  PMID: 24363565
Orobanche; taxonomy; critically endangered; Albania
21.  Oil-producing flowers within the Iridoideae (Iridaceae): evolutionary trends in the flowers of the New World genera 
Annals of Botany  2012;110(3):713-729.
Background and Aims
Oil-producing flowers related to oil-bee pollination are a major innovation in Neotropical and Mexican Iridaceae. In this study, phylogenetic relationships were investigated among a wide array of New World genera of the tribes Sisyrinchieae, Trimezieae and Tigridieae (Iridaceae: Iridoideae) and the evolution of floral glandular structures, which are predominantly trichomal elaiophores, was examined in relation to the diversification of New World Iridaceae.
Methods
Phylogenetic analyses based on seven molecular markers obtained from 97 species were conducted to produce the first extensive phylogeny of the New World tribes of subfamily Iridoideae. The resulting phylogenetic hypothesis was used to trace the evolutionary history of glandular structures present in the flowers of numerous species in each tribe. Hypotheses of differential diversification rates among lineages were also investigated using both topological and Binary-State Speciation and Extinction methods.
Key Results and Conclusions
Floral glandular structures and especially trichomal elaiophores evolved multiple times independently in the American tribes of Iridoideae. The distribution pattern of species displaying glandular trichomes across the phylogeny reveals lability in the pollination system and suggests that these structures may have played a significant role in the diversification of the Iridoideae on the American continent.
doi:10.1093/aob/mcs134
PMCID: PMC3400458  PMID: 22782239
Elaiophores; glandular trichomes; Iridoideae; nectaries; pollination systems; Sisyrinchieae; Tigridieae; Trimezieae
22.  Characterization of a Crabs Claw Gene in Basal Eudicot Species Epimedium sagittatum (Berberidaceae) 
The Crabs Claw (CRC) YABBY gene is required for regulating carpel development in angiosperms and has played an important role in nectary evolution during core eudicot speciation. The function or expression of CRC-like genes has been explored in two basal eudicots, Eschscholzia californica and Aquilegia formosa. To further investigate the function of CRC orthologous genes related to evolution of carpel and nectary development in basal eudicots, a CRC ortholog, EsCRC, was isolated and characterized from Epimedium sagittatum (Sieb. and Zucc.) Maxim. A phylogenetic analysis of EsCRC and previously identified CRC-like genes placed EsCRC within the basal eudicot lineage. Gene expression results suggest that EsCRC is involved in the development of sepals and carpels, but not nectaries. Phenotypic complementation of the Arabidopsis mutant crc-1 was achieved by constitutive expression of EsCRC. In addition, over-expression of EsCRC in Arabidopsis and tobacco gave rise to abaxially curled leaves. Transgenic results together with the gene expression analysis suggest that EsCRC may maintain a conserved function in carpel development and also play a novel role related to sepal formation. Absence of EsCRC and ElCRC expression in nectaries further indicates that nectary development in non-core eudicots is unrelated to expression of CRC-like genes.
doi:10.3390/ijms14011119
PMCID: PMC3565311  PMID: 23299438
Evo-Devo; nectary development; YABBY; CRC; basal eudicots
23.  Genomic tools development for Aquilegia: construction of a BAC-based physical map 
BMC Genomics  2010;11:621.
Background
The genus Aquilegia, consisting of approximately 70 taxa, is a member of the basal eudicot lineage, Ranuculales, which is evolutionarily intermediate between monocots and core eudicots, and represents a relatively unstudied clade in the angiosperm phylogenetic tree that bridges the gap between these two major plant groups. Aquilegia species are closely related and their distribution covers highly diverse habitats. These provide rich resources to better understand the genetic basis of adaptation to different pollinators and habitats that in turn leads to rapid speciation. To gain insights into the genome structure and facilitate gene identification, comparative genomics and whole-genome shotgun sequencing assembly, BAC-based genomics resources are of crucial importance.
Results
BAC-based genomic resources, including two BAC libraries, a physical map with anchored markers and BAC end sequences, were established from A. formosa. The physical map was composed of a total of 50,155 BAC clones in 832 contigs and 3939 singletons, covering 21X genome equivalents. These contigs spanned a physical length of 689.8 Mb (~2.3X of the genome) suggesting the complex heterozygosity of the genome. A set of 197 markers was developed from ESTs induced by drought-stress, or involved in anthocyanin biosynthesis or floral development, and was integrated into the physical map. Among these were 87 genetically mapped markers that anchored 54 contigs, spanning 76.4 Mb (25.5%) across the genome. Analysis of a selection of 12,086 BAC end sequences (BESs) from the minimal tiling path (MTP) allowed a preview of the Aquilegia genome organization, including identification of transposable elements, simple sequence repeats and gene content. Common repetitive elements previously reported in both monocots and core eudicots were identified in Aquilegia suggesting the value of this genome in connecting the two major plant clades. Comparison with sequenced plant genomes indicated a higher similarity to grapevine (Vitis vinifera) than to rice and Arabidopsis in the transcriptomes.
Conclusions
The A. formosa BAC-based genomic resources provide valuable tools to study Aquilegia genome. Further integration of other existing genomics resources, such as ESTs, into the physical map should enable better understanding of the molecular mechanisms underlying adaptive radiation and elaboration of floral morphology.
doi:10.1186/1471-2164-11-621
PMCID: PMC3091760  PMID: 21059242
24.  Salade malade: malignant ventricular arrhythmias due to an accidental intoxication with Aconitum napellus 
Netherlands Heart Journal  2008;16(3):96-99.
Intoxication with Aconitum napellus is rare in our regions. Aconite alkaloids can cause ventricular arrhythmia by a prolonged activation of sodium channels. Because the margin of safety is low between the analgesic and toxic dose, intoxication is not rare when Aconite is used in herbal medicine. We present a case in which a 39-year-old male was accidentally intoxicated with Aconite. Even though no antidote or adequate therapy is available he was successfully resuscitated. (Neth Heart J 2008;16:96-9.)
PMCID: PMC2266867  PMID: 18345331
intoxication; aconite; aconitum; cardiotoxic; resuscitation
25.  Circadian aspects of hyperthermia in mice induced by Aconitum napellus 
Pharmacognosy Magazine  2011;7(27):234-242.
Background:
Aconitum napellus (Acn) is used topically to relieve pain, itching and inflammation, and internally to reduce febrile states, among others. Any circadian time-related consequences of Acn administration are unknown. The objective of this study was to explore the effects of two doses of Acn on body temperature (BT) of mice treated at six different times over 24 hours.
Materials and Methods:
BALB/c female mice were housed in six chambers (six mice each) with air temperature 24 ± 3°C, humidity 60 ± 4%, and a 12-hours light (L)/12-hours dark cycle, but with L-onset staggered by 4 hours between chambers so that study at one external test time resulted in six test times (02, 06, 10, 14, 18 and 22 hours [h] after light onset). Rectal temperature (RT; in °C) was measured at baseline (B) and 1 hour after oral treatment with placebo (P) or two doses of Acn (6C and 30C, two studies each) in six studies over an 8 day span. The difference in RT for each mouse from the respective B + P timepoint mean RT was computed following each Acn treatment, and data from each of the six studies (original RT and difference from B + P) were analyzed for time-effect by analysis of variance (ANOVA) and for circadian rhythm by 24-hour cosine fitting.
Results:
A circadian rhythm in RT was found at B and after P (mean: 35.58°C vs. 35.69°C; peak: 15:31 h vs. 15:40 h) and after each Acn dose (30C or 6C). Acn induced hyperthermia and the overall change in BT was rhythmically significant for each dose (mean = +1.95°C vs. +1.70°C), with greatest hyperthermia observed during the L-span for each dose (peak = 08:56 h vs. 05:17 h).
Conclusion:
Acn administered around the clock induced hyperthermia overall and in a time-dependent manner, with greatest effects during the resting (L) span. Thus, time of day may significantly impact the outcome of Acn and other homeopathic treatments and should be considered in determining optimal dosing and treatment time(s) in order to increase the desired outcome and decrease undesired effects.
doi:10.4103/0973-1296.84238
PMCID: PMC3173899  PMID: 21969795
Aconite; Aconitum napellus; chronotherapy; circadian; homeopathy; hyperthermia; pharmacognosy

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