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1.  Floral Morphogenesis: Stochastic Explorations of a Gene Network Epigenetic Landscape 
PLoS ONE  2008;3(11):e3626.
In contrast to the classical view of development as a preprogrammed and deterministic process, recent studies have demonstrated that stochastic perturbations of highly non-linear systems may underlie the emergence and stability of biological patterns. Herein, we address the question of whether noise contributes to the generation of the stereotypical temporal pattern in gene expression during flower development. We modeled the regulatory network of organ identity genes in the Arabidopsis thaliana flower as a stochastic system. This network has previously been shown to converge to ten fixed-point attractors, each with gene expression arrays that characterize inflorescence cells and primordial cells of sepals, petals, stamens, and carpels. The network used is binary, and the logical rules that govern its dynamics are grounded in experimental evidence. We introduced different levels of uncertainty in the updating rules of the network. Interestingly, for a level of noise of around 0.5–10%, the system exhibited a sequence of transitions among attractors that mimics the sequence of gene activation configurations observed in real flowers. We also implemented the gene regulatory network as a continuous system using the Glass model of differential equations, that can be considered as a first approximation of kinetic-reaction equations, but which are not necessarily equivalent to the Boolean model. Interestingly, the Glass dynamics recover a temporal sequence of attractors, that is qualitatively similar, although not identical, to that obtained using the Boolean model. Thus, time ordering in the emergence of cell-fate patterns is not an artifact of synchronous updating in the Boolean model. Therefore, our model provides a novel explanation for the emergence and robustness of the ubiquitous temporal pattern of floral organ specification. It also constitutes a new approach to understanding morphogenesis, providing predictions on the population dynamics of cells with different genetic configurations during development.
PMCID: PMC2572848  PMID: 18978941
2.  Flower Development 
Flowers are the most complex structures of plants. Studies of Arabidopsis thaliana, which has typical eudicot flowers, have been fundamental in advancing the structural and molecular understanding of flower development. The main processes and stages of Arabidopsis flower development are summarized to provide a framework in which to interpret the detailed molecular genetic studies of genes assigned functions during flower development and is extended to recent genomics studies uncovering the key regulatory modules involved. Computational models have been used to study the concerted action and dynamics of the gene regulatory module that underlies patterning of the Arabidopsis inflorescence meristem and specification of the primordial cell types during early stages of flower development. This includes the gene combinations that specify sepal, petal, stamen and carpel identity, and genes that interact with them. As a dynamic gene regulatory network this module has been shown to converge to stable multigenic profiles that depend upon the overall network topology and are thus robust, which can explain the canalization of flower organ determination and the overall conservation of the basic flower plan among eudicots. Comparative and evolutionary approaches derived from Arabidopsis studies pave the way to studying the molecular basis of diverse floral morphologies.
PMCID: PMC3244948  PMID: 22303253
3.  Inside-out flowers of Lacandonia brasiliana (Triuridaceae) provide new insights into fundamental aspects of floral patterning 
PeerJ  2016;4:e1653.
Background and Aims. A recently described Brazilian species, Lacandonia brasiliana, shares with its longer established putative sister species from Mexico, L. schismatica, inverted floral patterning (carpels surrounding stamens) that is almost unique among angiosperms. We present a detailed ontogenetic study of L. brasiliana for comparison with other members of the tribe Triurideae (Triuridaceae) to explore the possible evolutionary origins of “inside-out” flowers.
Methods. Wild-source populations of L. brasiliana were compared morphologically and ontogenetically with related species of Triurideae, using light and scanning electron microscopy.
Key Results. Relatively few morphological differences separate flowers of L. brasiliana and L. schismatica. Both species have tepals with late-developing subapical appendages. In both species, the three central (almost sessile) anthers develop precociously with respect to the carpels; the anthers remain closed, and fertilization is achieved via pollen-tube growth from germinating pollen grains of the same cleistogamous flower. Carpels are initiated on fascicles.
Conclusions. The close similarity between the two Lacandonia species makes it unlikely that they arose independently from two separate homeotic transformation events; they could either represent sister species or two populations of a single disjunct species. Our study underlines the problematic generic and species boundaries within Triurideae. We present an evolutionary scenario of character evolution in Triuridaceae. The inside-out Lacandonia flower could have resulted from a stabilized homeotic transformation; this hypothesis is not in conflict with constrasting theories of the origin of the Triuridaceae flower, which coincided with a shift to unisexuality. The unisexual yet highly plastic flowers that are typical of Triuridaceae could have pre-adapted the origin of the extraordinary Lacandonia morphology.
PMCID: PMC4748704  PMID: 26870611
Lacandonia; Evolutionary transformation; Inside-out flowers; Mycoheterotrophs; Unisexuality; Triuridaceae; Pandanales
4.  De novo sequencing of the Hypericum perforatum L. flower transcriptome to identify potential genes that are related to plant reproduction sensu lato 
BMC Genomics  2015;16(1):254.
St. John’s wort (Hypericum perforatum L.) is a medicinal plant that produces important metabolites with antidepressant and anticancer activities. Recently gained biological information has shown that this species is also an attractive model system for the study of a naturally occurring form of asexual reproduction called apomixis, which allows cloning plants through seeds. In aposporic gametogenesis, one or multiple somatic cells belonging to the ovule nucellus change their fate by dividing mitotically and developing functionally unreduced embryo sacs by mimicking sexual gametogenesis. Although the introduction of apomixis into agronomically important crops could have revolutionary implications for plant breeding, the genetic control of this mechanism of seed formation is still not well understood for most of the model species investigated so far. We used Roche 454 technology to sequence the entire H. perforatum flower transcriptome of whole flower buds and single flower verticils collected from obligately sexual and unrelated highly or facultatively apomictic genotypes, which enabled us to identify RNAs that are likely exclusive to flower organs (i.e., sepals, petals, stamens and carpels) or reproductive strategies (i.e., sexual vs. apomictic).
Here we sequenced and annotated the flower transcriptome of H. perforatum with particular reference to reproductive organs and processes. In particular, in our study we characterized approximately 37,000 transcripts found expressed in male and/or female reproductive organs, including tissues or cells of sexual and apomictic flower buds. Ontological annotation was applied to identify major biological processes and molecular functions involved in flower development and plant reproduction. Starting from this dataset, we were able to recover and annotate a large number of transcripts related to meiosis, gametophyte/gamete formation, and embryogenesis, as well as genes that are exclusively or preferentially expressed in sexual or apomictic libraries. Real-Time RT-qPCR assays on pistils and anthers collected at different developmental stages from accessions showing alternative modes of reproduction were used to identify potential genes that are related to plant reproduction sensu lato in H. perforatum.
Our approach of sequencing flowers from two fully obligate sexual genotypes and two unrelated highly apomictic genotypes, in addition to different flower parts dissected from a facultatively apomictic accession, enabled us to analyze the complexity of the flower transcriptome according to its main reproductive organs as well as for alternative reproductive behaviors. Both annotation and expression data provided original results supporting the hypothesis that apomixis in H. perforatum relies upon spatial or temporal mis-expression of genes acting during female sexual reproduction. The present analyses aim to pave the way toward a better understanding of the molecular basis of flower development and plant reproduction, by identifying genes or RNAs that may differentiate or regulate the sexual and apomictic reproductive pathways in H. perforatum.
Electronic supplementary material
The online version of this article (doi:10.1186/s12864-015-1439-y) contains supplementary material, which is available to authorized users.
PMCID: PMC4451943  PMID: 25887758
Hypericum perforatum; Flower; Reproductive organs; Apomixis; Apospory
5.  Correlation between number and position of floral organs in Arabidopsis 
Annals of Botany  2011;108(1):123-131.
Background and Aims
The study of variation in number, position and type of floral organs may serve as a key to understanding the mechanisms underlying their variation, and will make it possible to improve the analysis of gene function in model plant species by means of a more accurate characterization of mutant phenotypes. The present analysis was carried out in order to understand the correlation between number and position of floral organs in Arabidopsis thaliana.
An analysis of number and position of organs in flowers of wild type as well as in a series of mutations with floral organ position alterations was carried out, using light and electron microscopy. Variation common to different genotypes was analysed by means of individual diagrams, upon which generalized diagrams depicting variation in number and position of organs, were built by superimposition.
Key Results and Conclusions
It is shown that in the Arabidopsis flower a correlation exists between positions of petals and sepals, as well as between positions of stamens and carpels, whereas the position of carpels does not seem to depend on number and position of petals and stamens. This suggests that the position of organs in the basal (sepals) and apical (carpels) parts of the flower are determined before that in the intermediate zone. This assumption is consistent with the results of mathematical modelling and is supposed to be the consequence of stem-cell activity in the flower.
PMCID: PMC3119622  PMID: 21693667
Flower organ position; Arabidopsis thaliana; flower development; floral patterning
6.  Functional recapitulation of transitions in sexual systems by homeosis during the evolution of dioecy in Thalictrum 
Sexual systems are highly variable in flowering plants and an important contributor to floral diversity. The ranunculid genus Thalictrum is especially well-suited to study evolutionary transitions in sexual systems. Homeotic transformation of sexual organs (stamens and carpels) is a plausible mechanism for the transition from hermaphroditic to unisexual flowers in this lineage because flowers of dioecious species develop unisexually from inception. The single-copy gene PISTILLATA (PI) constitutes a likely candidate for rapid switches between stamen and carpel identity. Here, we first characterized the expression pattern of all B class genes in the dioecious species T. dioicum. As expected, all B class orthologs are expressed in stamens from the earliest stages. Certain AP3 lineages were also expressed late in sepal development. We then tested whether orthologs of PI could potentially control sexual system transitions in Thalictrum, by knocking-down their expression in T. dioicum and the hermaphroditic species T. thalictroides. In T. dioicum, we found that ThdPI-1/2 silencing caused stamen primordia to develop into carpels, resulting in male to female flower conversions. In T. thalictroides, we found that ThtPI silencing caused stamen primordia to develop into supernumerary carpels, resulting in hermaphroditic to female flower conversions. These phenotypes illustrate the ability for homeotic mutations to bring about sudden and potentially adaptive changes by altering the function of a single gene. We propose a two-step evolutionary model where transitions from hermaphroditic to unisexual plants in Thalictrum result from two independent mutations at a B class gene locus. Our PI knockdown experiments in T. thalictroides recapitulate the second step in this model: the evolution of female plants as a result of a loss-of-function mutation in a B class gene.
PMCID: PMC3842162  PMID: 24348491
B class genes; PISTILLATA; VIGS; RNAi; ranunculid; ABC model; sex determination; MADS box genes
7.  Tracking the development of the petaloid fertile stamen in Canna indica: insights into the origin of androecial petaloidy in the Zingiberales 
AoB Plants  2013;5:plt009.
The order Zingiberales comprises ∼2500 species of tropical to subtropical plants, including agriculturally (e.g. banana, ginger) and horticulturally (e.g. cannas, heliconias, bird-of-paradise) important plants. Throughout the evolution of this order, the stamens have been modified from the ancestral filamentous structures that produce pollen (seen in Banana flowers) to petal-like structures that no longer bear pollen sacs (seen in Canna flowers). This results in a reduction of pollen, but an effective increase in the overall size of the floral display and perhaps in the efficacy of specialized pollinators by converting stamens into ‘petals’. This study investigates the genetic mechanisms that are involved in making petal-like structures in place of pollen-producing stamens.
Flowers of the order Zingiberales demonstrate a remarkable trend of reduction in the number of fertile stamens; from five or six fertile, filamentous stamens bearing two thecae each in Musaceae and Strelitziaceae to just a single petaloid stamen bearing a single theca in Cannaceae and Marantaceae. As one progresses from ancestral to derived floral forms, 5–6 fertile stamens are replaced by 4–5 petaloid staminodes. In Cannaceae and Costaceae, all members of the androecial whorls exhibit petaloidy, including the fertile stamen. In Costaceae, a single fertile stamen develops two thecae embedded on a broad petaloid appendage, while in Cannaceae the single fertile stamen is further reduced to a single theca with a prominent, expanded petaloid appendage. Whether petaloidy of the fertile stamen is a synapomorphy of the entire ginger clade (including Cannaceae, Costaceae, Zingiberaceae and Marantaceae), or the result of independent convergent evolution in Cannaceae, Costaceae, and some Zingiberaceae, is unclear. We combine a developmental series of the formation of the petaloid fertile stamen in Canna indica with data on the expression of B- and C-class floral organ identity genes to elucidate the organogenetic identity of the petaloid stamen and staminodes. Our data indicate that the single fertile theca in C. indica and its petaloid appendage are derived from one-half of the primordium of a single stamen, with no contribution from the remaining part of the stamen (i.e. the second theca primordium) which aborts early in development. The petaloid appendage expands later, and develops from the position of the filament/connective of the developing theca. Floral identity gene expression shows that petal identity genes (i.e. B-class genes) are expressed in all floral organs studied while C-class gene AG-1 is expressed in an increasing gradient from sepals to gynoecium, and AG-2 is expressed in all floral organs except the petals. The canonical model for molecular specification of floral organ identity is not sufficient to explain petaloidy in the androecial whorl in Canna sp. Further studies understanding the regulation of gene networks are required.
PMCID: PMC3608240  PMID: 23539493
Canna; evo-devo; floral development; MADS-box genes; petaloid stamens; petaloidy; Zingiberales
8.  'Who's who' in two different flower types of Calluna vulgaris (Ericaceae): morphological and molecular analyses of flower organ identity 
BMC Plant Biology  2009;9:148.
The ornamental crop Calluna vulgaris is of increasing importance to the horticultural industry in the northern hemisphere due to a flower organ mutation: the flowers of the 'bud-flowering' phenotype remain closed i.e. as buds throughout the total flowering period and thereby maintain more colorful flowers for a longer period of time than the wild-type. This feature is accompanied and presumably caused by the complete lack of stamens. Descriptions of this botanical particularity are inconsistent and partially conflicting. In order to clarify basic questions of flower organ identity in general and stamen loss in detail, a study of the wild-type and the 'bud-flowering' flower type of C. vulgaris was initiated.
Flowers were examined by macro- and microscopic techniques. Organ development was investigated comparatively in both the wild-type and the 'bud-flowering' type by histological analyses. Analysis of epidermal cell surface structure of vegetative tissues and perianth organs using scanning electron microscopy revealed that in wild-type flowers the outer whorls of colored organs may be identified as sepals, while the inner ones may be identified as petals. In the 'bud-flowering' type, two whorls of sepals are directly followed by the gynoecium. Both, petals and stamens, are completely missing in this flower type. The uppermost whorl of green leaves represents bracts in both flower types.
In addition, two MADS-box genes (homologs of AP3/DEF and SEP1/2) were identified in C. vulgaris using RACE-PCR. Expression analysis by qRT-PCR was conducted for both genes in leaves, bracts, sepals and petals. These experiments revealed an expression pattern supporting the organ classification based on morphological characteristics.
Organ identity in both wild-type and 'bud-flowering' C. vulgaris was clarified using a combination of microscopic and molecular methods. Our results for bract, sepal and petal organ identity are supported by the 'ABCDE model'. However, loss of stamens in the 'bud-flowering' phenotype is an exceptional flower organ modification that cannot be explained by modified spatial expression of known organ identity genes.
PMCID: PMC2803492  PMID: 20003430
9.  An atlas of gene regulatory networks reveals multiple three-gene mechanisms for interpreting morphogen gradients 
Although >450 different topologies can achieve the same multicellular patterning function, they can be grouped into six main classes, which operate using different underlying dynamics.Alternative designs for the same functions can therefore split into two types: (a) topology alterations that retain the same underlying dynamics and (b) alterations that utilize a completely different underlying dynamical mechanism.This segregation of networks into distinct dynamical mechanisms can be revealed by the shape of the topology atlas itself.Cell–cell communication is not usually part of the causal mechanism underlying a band-pass response during morphogen interpretation, but it can tune the result or increase robustness.
Understanding how gene regulatory networks (GRNs) achieve particular biological functions is a central question in systems biology. Systems biology promises to go beyond a case-by-case understanding of individual networks to map out the complete design space of mechanistic possibilities that underlie biological functions. Can such maps serve as useful theoretical frameworks in which to explore the general design principles for these functions? Towards addressing these questions, we created the first design space for a morphogen interpretation function.
In order to generate a design space for such a function, we enumerated all possible wiring designs of GRNs consisting of three genes and tested their ability to perform one particular morphogen interpretation function; stripe formation, as it represents a simplified form of the much studied French flag problem and is a commonly found gene expression pattern (Figure 1A). We found that only 5% of GRNs had the ability to generate a single stripe of gene expression when simulated with a fixed morphogen input in a one-dimensional model.
We hypothesized that the core mechanisms for producing the stripe of gene expression should be represented by topologies that contain only the necessary and sufficient gene–gene interactions for that function. Hence, we utilized the notions of complexity and neighborhood to generate a complexity atlas. GRNs of such an atlas (represented by nodes) are considered neighbors if they differ by a single gene–gene interaction (neighboring GRN nodes are connected by edges). Such a metagraph (graph of graphs) can then be reorganized using complexity (number of gene–gene interactions) to determine a GRNs position in the y axis, whereas GRNs are spaced in the x axis with the aim of reducing edge crossing (Figure 5A). This reorganization reveals a striking structure, where ‘stalactites' of complexity can be seen protruding from the bottom of the atlas. Each of these stalactites converges on a single ‘core' topology that by extensive analysis we find represents a distinct mechanism.
The mechanisms employ a diverse range of distinct space–time behaviors, and the underlying core topologies display design features such as modularity and feed-forward. We mapped the mechanisms to the complexity atlas by analyzing how each particular GRN of the atlas was working. The GRNs functioning via the different mechanisms are highlighted by the different colors in Figure 5A. Mechanisms thus occupy large regions of separated topology space, suggesting them to be discrete. Analyzing transitions between mechanisms through parameter space confirms this to be the case.
We find that three of the mechanisms are employed in real patterning systems, including both blastoderm patterning in Drosophila and mesoderm specification in Xenopus (Figure 5B). The remaining three mechanisms are thus candidates for employment in other patterning systems. We explored the performance features of these mechanisms, which suggest that some have features such as robustness to parameter variation that make them highly likely to be employed in particular patterning contexts.
Only one of the six-core mechanisms absolutely requires cell–cell communication for functionality, prompting us to predict that cell–cell communication will rarely be responsible for the basic dose response of morphogen interpretation networks. However, we show how cell–cell communication has an important role in robust stripe generation in the face of a noisy morphogen input and in fine tuning the quantitative details of stripe patterning.
In summary, the complexity atlas approach is an amendable approach to any system with a clear genotype–function relationship. We demonstrate how certain functions such as morphogen interpretation may have a range of potential solutions in contrast to previous studies that analyzed more constrained functions. Furthermore, we demonstrate how such an approach can be utilized to define a ‘design space' for a given biological function that describes the different mechanistic possibilities and how they relate to one another (Figure 5). Such a design space can be used practically as a guide to discern which patterning mechanisms are likely be at work in a particular context throwing up less intuitive possibilities with powerful performance features.
The interpretation of morphogen gradients is a pivotal concept in developmental biology, and several mechanisms have been proposed to explain how gene regulatory networks (GRNs) achieve concentration-dependent responses. However, the number of different mechanisms that may exist for cells to interpret morphogens, and the importance of design features such as feedback or local cell–cell communication, is unclear. A complete understanding of such systems will require going beyond a case-by-case analysis of real morphogen interpretation mechanisms and mapping out a complete GRN ‘design space.' Here, we generate a first atlas of design space for GRNs capable of patterning a homogeneous field of cells into discrete gene expression domains by interpreting a fixed morphogen gradient. We uncover multiple very distinct mechanisms distributed discretely across the atlas, thereby expanding the repertoire of morphogen interpretation network motifs. Analyzing this diverse collection of mechanisms also allows us to predict that local cell–cell communication will rarely be responsible for the basic dose-dependent response of morphogen interpretation networks.
PMCID: PMC3010108  PMID: 21045819
design space; gene network; morphogen; patterning; systems biology
10.  Comparative Transcriptional Profiling Provides Insights into the Evolution and Development of the Zygomorphic Flower of Vicia sativa (Papilionoideae) 
PLoS ONE  2013;8(2):e57338.
Vicia sativa (the common vetch) possesses a predominant zygomorphic flower and belongs to the subfamily Papilionoideae, which is related to Arabidopsis thaliana in the eurosid II clade of the core eudicots. Each vetch flower consists of 21 concentrically arranged organs: the outermost five sepals, then five petals and ten stamens, and a single carpel in the center.
Methodology/Principal Findings
We explored the floral transcriptome to examine a genome-scale genetic model of the zygomorphic flower of vetch. mRNA was obtained from an equal mixture of six floral organs, leaves and roots. De novo assembly of the vetch transcriptome using Illumina paired-end technology produced 71,553 unigenes with an average length of 511 bp. We then compared the expression changes in the 71,553 unigenes in the eight independent organs through RNA-Seq Quantification analysis. We predominantly analyzed gene expression patterns specific to each floral organ and combinations of floral organs that corresponded to the traditional ABC model domains. Comparative analyses were performed in the floral transcriptomes of vetch and Arabidopsis, and genomes of vetch and Medicago truncatula.
Our comparative analysis of vetch and Arabidopsis showed that the vetch flowers conform to a strict ABC model. We analyzed the evolution and expression of the TCP gene family in vetch at a whole-genome level, and several unigenes specific to three different vetch petals, which might offer some clues toward elucidating the molecular mechanisms underlying floral zygomorphy. Our results provide the first insights into the genome-scale molecular regulatory network that controls the evolution and development of the zygomorphic flower in Papilionoideae.
PMCID: PMC3578871  PMID: 23437373
11.  Simulation of Organ Patterning on the Floral Meristem Using a Polar Auxin Transport Model 
PLoS ONE  2012;7(1):e28762.
An intriguing phenomenon in plant development is the timing and positioning of lateral organ initiation, which is a fundamental aspect of plant architecture. Although important progress has been made in elucidating the role of auxin transport in the vegetative shoot to explain the phyllotaxis of leaf formation in a spiral fashion, a model study of the role of auxin transport in whorled organ patterning in the expanding floral meristem is not available yet. We present an initial simulation approach to study the mechanisms that are expected to play an important role. Starting point is a confocal imaging study of Arabidopsis floral meristems at consecutive time points during flower development. These images reveal auxin accumulation patterns at the positions of the organs, which strongly suggests that the role of auxin in the floral meristem is similar to the role it plays in the shoot apical meristem. This is the basis for a simulation study of auxin transport through a growing floral meristem, which may answer the question whether auxin transport can in itself be responsible for the typical whorled floral pattern. We combined a cellular growth model for the meristem with a polar auxin transport model. The model predicts that sepals are initiated by auxin maxima arising early during meristem outgrowth. These form a pre-pattern relative to which a series of smaller auxin maxima are positioned, which partially overlap with the anlagen of petals, stamens, and carpels. We adjusted the model parameters corresponding to properties of floral mutants and found that the model predictions agree with the observed mutant patterns. The predicted timing of the primordia outgrowth and the timing and positioning of the sepal primordia show remarkable similarities with a developing flower in nature.
PMCID: PMC3264561  PMID: 22291882
12.  Floral development and vascularization help to explain merism evolution in Paepalanthus (Eriocaulaceae, Poales) 
PeerJ  2016;4:e2811.
Flowers in Eriocaulaceae, a monocot family that is highly diversified in Brazil, are generally trimerous, but dimerous flowers occur in Paepalanthus and a few other genera. The floral merism in an evolutionary context, however, is unclear. Paepalanthus encompasses significant morphological variation leading to a still unresolved infrageneric classification. Ontogenetic comparative studies of infrageneric groups in Paepalanthus and in Eriocaulaceae are lacking, albeit necessary to establish evolution of characters such as floral merism and their role as putative synapomorphies.
We studied the floral development and vascularization of eight species of Paepalanthus that belong to distinct clades in which dimery occurs, using light and scanning electron microscopies.
Floral ontogeny in dimerous Paepalanthus shows lateral sepals emerging simultaneously and late-developing petals. The outer whorl of stamens is absent in all flowers examined here. The inner whorl of stamens becomes functional in staminate flowers and is reduced to staminodes in the pistillate ones. In pistillate flowers, vascular bundles reach the staminodes. Ovary vascularization shows ventral bundles in a commissural position reaching the synascidiate portion of the carpels. Three gynoecial patterns are described for the studied species: (1) gynoecium with a short style, two nectariferous branches and two long stigmatic branches, in most species; (2) gynoecium with a long style, two nectariferous branches and two short stigmatic branches, in P. echinoides; and (3) gynoecium with long style, absent nectariferous branches and two short stigmatic branches, in P. scleranthus.
Floral development of the studied species corroborates the hypothesis that the sepals of dimerous flowers of Paepalanthus correspond to the lateral sepals of trimerous flowers. The position and vascularization of floral parts also show that, during dimery evolution in Paepalanthus, a flower sector comprising the adaxial median sepal, a lateral petal, a lateral stamen and the adaxial median carpel was lost. In the staminate flower, the outer whorl of staminodes, previously reported by different authors, is correctly described as the apical portion of the petals and the pistillodes are reinterpreted as carpellodes. The occurrence of fused stigmatic branches and protected nectariferous carpellodes substantiates a close relationship between P. sect. Conodiscus and P. subg. Thelxinoë. Free stigmatic branches and exposed carpellodes substantiate a close relationship between P. sect. Diphyomene, P. sect. Eriocaulopsis and P. ser. Dimeri. Furthermore, the loss of nectariferous branches may have occurred later than the fusion of stigmatic branches in the clade that groups P. subg. Thelxinoë and P. sect. Conodiscus.
PMCID: PMC5180585  PMID: 28028476
Dimery; Floral anatomy; Monocotyledons; Floral ontogeny; Paepalanthoideae
13.  Floral Development of Berberidopsis corallina: a Crucial Link in the Evolution of Flowers in the Core Eudicots 
Annals of Botany  2004;94(5):741-751.
• Background and Aims On the basis of molecular evidence Berberidopsidaceae have been linked with Aextoxicaceae in an order Berberidopsidales at the base of the core Eudicots. The floral development of Berberidopsis is central to the understanding of the evolution of floral configurations at the transition of the basal Eudicots to the core Eudicots. It lies at the transition of trimerous or dimerous, simplified apetalous forms into pentamerous, petaliferous flowers.
• Methods The floral ontogeny of Berberidopsis was studied with a scanning electron microscope.
• Key Results Flowers are grouped in terminal racemes with variable development. The relationship between the number of tepals, stamens and carpels is more or less fixed and floral initiation follows a strict 2/5 phyllotaxis. Two bracteoles, 12 tepals, eight stamens and three carpels are initiated in a regular sequence. The number of stamens can be increased by a doubling of stamen positions.
• Conclusions The floral ontogeny of Berberidopsis provides support for the shift in floral bauplan from the basal Eudicots to the core Eudicots as a transition of a spiral flower with a 2/5 phyllotaxis to pentamerous flowers with two perianth whorls, two stamen whorls and a single carpel whorl. The differentiation of sepals and petals from bracteotepals is discussed and a comparison is made with other Eudicots with a similar configuration and development. Depending on the resolution of the relationships among the basalmost core Eudicots it is suggested that Berberidopsis either represents a critical stage in the evolution of pentamerous flowers of major clades of Eudicots, or has a floral prototype that may be at the base of evolution of flowers of other core Eudicots. The distribution of a floral Bauplan in other clades of Eudicots similar to Berberidopsidales is discussed.
PMCID: PMC4242220  PMID: 15451722
Aextoxicon; Berberidopsidales; Berberidopsis; core Eudicots; Streptothamnus; bracteotepals; floral development, petals; phylogeny; phyllotaxis; scanning electron microscope
14.  Reshaping the epigenetic landscape during early flower development: induction of attractor transitions by relative differences in gene decay rates 
BMC Systems Biology  2015;9:20.
Gene regulatory network (GRN) dynamical models are standard systems biology tools for the mechanistic understanding of developmental processes and are enabling the formalization of the epigenetic landscape (EL) model.
In this work we propose a modeling framework which integrates standard mathematical analyses to extend the simple GRN Boolean model in order to address questions regarding the impact of gene specific perturbations in cell-fate decisions during development.
We systematically tested the propensity of individual genes to produce qualitative changes to the EL induced by modification of gene characteristic decay rates reflecting the temporal dynamics of differentiation stimuli. By applying this approach to the flower specification GRN (FOS-GRN) we uncovered differences in the functional (dynamical) role of their genes. The observed dynamical behavior correlates with biological observables. We found a relationship between the propensity of undergoing attractor transitions between attraction basins in the EL and the direction of differentiation during early flower development - being less likely to induce up-stream attractor transitions as the course of development progresses. Our model also uncovered a potential mechanism at play during the transition from EL basins defining inflorescence meristem to those associated to flower organs meristem. Additionally, our analysis provided a mechanistic interpretation of the homeotic property of the ABC genes, being more likely to produce both an induced inter-attractor transition and to specify a novel attractor. Finally, we found that there is a close relationship between a gene’s topological features and its propensity to produce attractor transitions.
The study of how the state-space associated with a dynamical model of a GRN can be restructured by modulation of genes’ characteristic expression times is an important aid for understanding underlying mechanisms occurring during development. Our contribution offers a simple framework to approach such problem, as exemplified here by the case of flower development. Different GRN models and the effect of diverse inductive signals can be explored within the same framework. We speculate that the dynamical role of specific genes within a GRN, as uncovered here, might give information about which genes are more likely to link a module to other regulatory circuits and signaling transduction pathways.
Electronic supplementary material
The online version of this article (doi:10.1186/s12918-015-0166-y) contains supplementary material, which is available to authorized users.
PMCID: PMC4438470  PMID: 25967891
Gene regulatory network; Epigenetic landscape; Attractor landscape; Differentiation; Flower development; Attractor transitions
15.  Within and between Whorls: Comparative Transcriptional Profiling of Aquilegia and Arabidopsis 
PLoS ONE  2010;5(3):e9735.
The genus Aquilegia is an emerging model system in plant evolutionary biology predominantly because of its wide variation in floral traits and associated floral ecology. The anatomy of the Aquilegia flower is also very distinct. There are two whorls of petaloid organs, the outer whorl of sepals and the second whorl of petals that form nectar spurs, as well as a recently evolved fifth whorl of staminodia inserted between stamens and carpels.
Methodology/Principal Findings
We designed an oligonucleotide microarray based on EST sequences from a mixed tissue, normalized cDNA library of an A. formosa x A. pubescens F2 population representing 17,246 unigenes. We then used this array to analyze floral gene expression in late pre-anthesis stage floral organs from a natural A. formosa population. In particular, we tested for gene expression patterns specific to each floral whorl and to combinations of whorls that correspond to traditional and modified ABC model groupings. Similar analyses were performed on gene expression data of Arabidopsis thaliana whorls previously obtained using the Ath1 gene chips (data available through The Arabidopsis Information Resource).
Our comparative gene expression analyses suggest that 1) petaloid sepals and petals of A. formosa share gene expression patterns more than either have organ-specific patterns, 2) petals of A. formosa and A. thaliana may be independently derived, 3) staminodia express B and C genes similar to stamens but the staminodium genetic program has also converged on aspects of the carpel program and 4) staminodia have unique up-regulation of regulatory genes and genes that have been implicated with defense against microbial infection and herbivory. Our study also highlights the value of comparative gene expression profiling and the Aquilegia microarray in particular for the study of floral evolution and ecology.
PMCID: PMC2843724  PMID: 20352114
16.  Flower Development and Perianth Identity Candidate Genes in the Basal Angiosperm Aristolochia fimbriata (Piperales: Aristolochiaceae) 
Aristolochia fimbriata (Aristolochiaceae: Piperales) exhibits highly synorganized flowers with a single convoluted structure forming a petaloid perianth that surrounds the gynostemium, putatively formed by the congenital fusion between stamens and the upper portion of the carpels. Here we present the flower development and morphology of A. fimbriata, together with the expression of the key regulatory genes that participate in flower development, particularly those likely controlling perianth identity. A. fimbriata is a member of the magnoliids, and thus gene expression detected for all ABCE MADS-box genes in this taxon, can also help to elucidate patterns of gene expression prior the independent duplications of these genes in eudicots and monocots. Using both floral development and anatomy in combination with the isolation of MADS-box gene homologs, gene phylogenetic analyses and expression studies (both by reverse transcription PCR and in situ hybridization), we present hypotheses on floral organ identity genes involved in the formation of this bizarre flower. We found that most MADS-box genes were expressed in vegetative and reproductive tissues with the exception of AfimSEP2, AfimAGL6, and AfimSTK transcripts that are only found in flowers and capsules but are not detected in leaves. Two genes show ubiquitous expression; AfimFUL that is found in all floral organs at all developmental stages as well as in leaves and capsules, and AfimAG that has low expression in leaves and is found in all floral organs at all stages with a considerable reduction of expression in the limb of anthetic flowers. Our results indicate that expression of AfimFUL is indicative of pleiotropic roles and not of a perianth identity specific function. On the other hand, expression of B-class genes, AfimAP3 and AfimPI, suggests their conserved role in stamen identity and corroborates that the perianth is sepal and not petal-derived. Our data also postulates an AGL6 ortholog as a candidate gene for sepal identity in the Aristolochiaceae and provides testable hypothesis for a modified ABCE model in synorganized magnoliid flowers.
PMCID: PMC4675851  PMID: 26697047
AGAMOUS-like6; APETALA3; Aristolochia fimbriata; FRUITFULL; magnoliids; MADS-box genes; perianth; PISTILLATA
17.  Target Genes of the MADS Transcription Factor SEPALLATA3: Integration of Developmental and Hormonal Pathways in the Arabidopsis Flower 
PLoS Biology  2009;7(4):e1000090.
The molecular mechanisms by which floral homeotic genes act as major developmental switches to specify the identity of floral organs are still largely unknown. Floral homeotic genes encode transcription factors of the MADS-box family, which are supposed to assemble in a combinatorial fashion into organ-specific multimeric protein complexes. Major mediators of protein interactions are MADS-domain proteins of the SEPALLATA subfamily, which play a crucial role in the development of all types of floral organs. In order to characterize the roles of the SEPALLATA3 transcription factor complexes at the molecular level, we analyzed genome-wide the direct targets of SEPALLATA3. We used chromatin immunoprecipitation followed by ultrahigh-throughput sequencing or hybridization to whole-genome tiling arrays to obtain genome-wide DNA-binding patterns of SEPALLATA3. The results demonstrate that SEPALLATA3 binds to thousands of sites in the genome. Most potential target sites that were strongly bound in wild-type inflorescences are also bound in the floral homeotic agamous mutant, which displays only the perianth organs, sepals, and petals. Characterization of the target genes shows that SEPALLATA3 integrates and modulates different growth-related and hormonal pathways in a combinatorial fashion with other MADS-box proteins and possibly with non-MADS transcription factors. In particular, the results suggest multiple links between SEPALLATA3 and auxin signaling pathways. Our gene expression analyses link the genomic binding site data with the phenotype of plants expressing a dominant repressor version of SEPALLATA3, suggesting that it modulates auxin response to facilitate floral organ outgrowth and morphogenesis. Furthermore, the binding of the SEPALLATA3 protein to cis-regulatory elements of other MADS-box genes and expression analyses reveal that this protein is a key component in the regulatory transcriptional network underlying the formation of floral organs.
Author Summary
Most regulatory genes encode transcription factors, which modulate gene expression by binding to regulatory sequences of their target genes. In plants in particular, which genes are directly controlled by these transcription factors, and the molecular mechanisms of target gene recognition in vivo, are still largely unexplored. One of the best-understood developmental processes in plants is flower development. In different combinations, transcription factors of the MADS-box family control the identities of the different types of floral organs: sepals, petals, stamens, and carpels. Here, we present the first genome-wide analysis of binding sites of a MADS-box transcription factor in plants. We show that the MADS-domain protein SEPALLATA3 (SEP3) binds to the regulatory regions of thousands of potential target genes, many of which are also transcription factors. We provide insight into mechanisms of DNA recognition by SEP3, and suggest roles for other transcription factor families in SEP3 target gene regulation. In addition to effects on genes involved in floral organ identity, our data suggest that SEP3 binds to, and modulates, the transcription of target genes involved in hormonal signaling pathways.
The key floral regulator SEPALLATA3 binds to the promoters of a large number of potential direct target genes to integrate different growth-related and hormonal pathways in flower development.
PMCID: PMC2671559  PMID: 19385720
18.  Leaf Development 
The shoot system is the basic unit of development of seed plants and is composed of a leaf, a stem, and a lateral bud that differentiates into a lateral shoot. The most specialized organ in angiosperms, the flower, can be considered to be part of the same shoot system since floral organs, such as the sepal, petal, stamen, and carpel, are all modified leaves. Scales, bracts, and certain kinds of needle are also derived from leaves. Thus, an understanding of leaf development is critical to an understanding of shoot development. Moreover, leaves play important roles in photosynthesis, respiration and photoperception. Thus, a full understanding of leaves is directly related to a full understanding of seed plants.
The details of leaf development remain unclear. The difficulties encountered in studies of leaf development, in particular in dicotyledonous plants such as Arabidopsis thaliana (L.) Henyn., are derived from the complex process of leaf development, during which the division and elongation of cells occur at the same time and in the same region of the leaf primordium (Maksymowych, 1963; Poethig and Sussex, 1985). Thus, we cannot divide the entire process into unit processes in accordance with the tenets of classical anatomy.
Genetic approaches in Arabidopsis, a model plant (Meyerowitz and Pruitt, 1985), have provided a powerful tool for studies of mechanisms of leaf development in dicotyledonous plants, and various aspects of the mechanisms that control leaf development have been revealed in recent developmental and molecular genetic studies of Arabidopsis (for reviews, see Tsukaya, 1995 and 1998; Van Lijsebettens and Clarke, 1998; Sinha, 1999; Van Volkenburgh, 1999; Tsukaya, 2000; Byrne et al., 2001; Dengler and Kang, 2001; Dengler and Tsukaya, 2001; Tsukaya, 2001). In this review, we shall examine the information that is currently available about various mechanisms of leaf development in Arabidopsis. Vascular patterning is also an important factor in the determination of leaf shape, and this topic is reviewed in this resource by Turner (see also Dengler and Kang, 2001). The interested reader is also referred to work on the basic characterization of the vascular patterning in foliage leaves of Arabidopsis has been carried out by Candela et al. (1999) and Semiarti et al. (2001). For terminology, see Fig. 1.
PMCID: PMC3243299  PMID: 22303217
19.  Temporal-Spatial Transcriptome Analyses Provide Insights into the Development of Petaloid Androecium in Canna indica 
Canna indica (Zingiberales) is one of the most important ornamental species characterized with beautiful petaloid staminodes, which are considered to evolve from stamens. However, the genetic basis for the development of petaloid staminodes remains unclear largely because the genomic sequences are not available. By using RNA-Seq, we sequenced the transcripts in the flower of C. indica, and quantified the temporal gene expressions in flower primordium and differentiated flower, as well as the spatial gene expressions in petal and petaloid staminode. In total, 118,869 unigenes were assembled, among which 67,299 unigenes were annotated. Quantification analysis identified the differentially expressed genes in the temporal and spatial two comparisons, based on which, Gene Ontology enrichment analysis highlighted the representative terms in each sample, such as specification of organ number in flower primordium, growth in differentiated flower, secondary cell wall biogenesis in petal and cell division in petaloid staminode. Among the 51 analyzed MADS-box unigenes, 37 were up-regulated in differentiated flower compared with those in flower primordium. A-class unigenes were expressed higher in petal than in petaloid staminode, and C-class unigenes were expressed oppositely, whereas B-class unigenes demonstrated close expression levels in these two organs, indicating that petaloid staminode retains stamen identity to some degree. In situ hybridization provided more detailed expression patterns of these unigenes, and revealed the extended expression of B-class to the carpel at later stages when the style turned flat. These results constitute a preliminary basis for the study of flower development in C. indica and can be applied in further study of the evolution of Zingiberales.
PMCID: PMC4987385  PMID: 27582744
transcriptome; RNA-Seq; petaloid staminode; Zingiberales; Canna indica; ABC model
20.  A Regulatory Network for Coordinated Flower Maturation 
PLoS Genetics  2012;8(2):e1002506.
For self-pollinating plants to reproduce, male and female organ development must be coordinated as flowers mature. The Arabidopsis transcription factors AUXIN RESPONSE FACTOR 6 (ARF6) and ARF8 regulate this complex process by promoting petal expansion, stamen filament elongation, anther dehiscence, and gynoecium maturation, thereby ensuring that pollen released from the anthers is deposited on the stigma of a receptive gynoecium. ARF6 and ARF8 induce jasmonate production, which in turn triggers expression of MYB21 and MYB24, encoding R2R3 MYB transcription factors that promote petal and stamen growth. To understand the dynamics of this flower maturation regulatory network, we have characterized morphological, chemical, and global gene expression phenotypes of arf, myb, and jasmonate pathway mutant flowers. We found that MYB21 and MYB24 promoted not only petal and stamen development but also gynoecium growth. As well as regulating reproductive competence, both the ARF and MYB factors promoted nectary development or function and volatile sesquiterpene production, which may attract insect pollinators and/or repel pathogens. Mutants lacking jasmonate synthesis or response had decreased MYB21 expression and stamen and petal growth at the stage when flowers normally open, but had increased MYB21 expression in petals of older flowers, resulting in renewed and persistent petal expansion at later stages. Both auxin response and jasmonate synthesis promoted positive feedbacks that may ensure rapid petal and stamen growth as flowers open. MYB21 also fed back negatively on expression of jasmonate biosynthesis pathway genes to decrease flower jasmonate level, which correlated with termination of growth after flowers have opened. These dynamic feedbacks may promote timely, coordinated, and transient growth of flower organs.
Author Summary
Perfect flowers have both male organs that produce and release pollen and female organs that make and harbor seeds. Flowers also often attract pollinators using visual or chemical signals. So that male, female, and pollinator attraction functions occur at the right time, flower organs must grow and mature in a coordinated fashion. In the model self-pollinating plant Arabidopsis, a transcriptional network regulates genes that ensure coordinated growth of different flower organs, as well as pollen release and gynoecium (female) competence to support pollination. This network also regulates nectary development and production of volatile chemicals that may attract or repel insects. We have studied growth, chemical signal levels, and gene expression in mutants affected in components of this network, in order to determine how flower growth is controlled. Several plant hormones act in a cascade that promotes flower maturation. Moreover, regulatory feedback loops affect the timing and extent of developmental steps. Positive feedbacks may ensure that the development of different flower organs is coordinated and rapid, whereas negative feedbacks may allow growth to cease once flowers have opened. Our results provide a framework to understand how flower opening and reproduction are coordinated in Arabidopsis and other flowering plants.
PMCID: PMC3276552  PMID: 22346763
21.  Transcriptome Analysis of Flower Sex Differentiation in Jatropha curcas L. Using RNA Sequencing 
PLoS ONE  2016;11(2):e0145613.
Jatropha curcas is thought to be a promising biofuel material, but its yield is restricted by a low ratio of instaminate / staminate flowers (1/10-1/30). Furthermore, valuable information about flower sex differentiation in this plant is scarce. To explore the mechanism of this process in J. curcas, transcriptome profiling of flower development was carried out, and certain genes related with sex differentiation were obtained through digital gene expression analysis of flower buds from different phases of floral development.
After Illumina sequencing and clustering, 57,962 unigenes were identified. A total of 47,423 unigenes were annotated, with 85 being related to carpel and stamen differentiation, 126 involved in carpel and stamen development, and 592 functioning in the later development stage for the maturation of staminate or instaminate flowers. Annotation of these genes provided comprehensive information regarding the sex differentiation of flowers, including the signaling system, hormone biosynthesis and regulation, transcription regulation and ubiquitin-mediated proteolysis. A further expression pattern analysis of 15 sex-related genes using quantitative real-time PCR revealed that gibberellin-regulated protein 4-like protein and AMP-activated protein kinase are associated with stamen differentiation, whereas auxin response factor 6-like protein, AGAMOUS-like 20 protein, CLAVATA1, RING-H2 finger protein ATL3J, auxin-induced protein 22D, and r2r3-myb transcription factor contribute to embryo sac development in the instaminate flower. Cytokinin oxidase, Unigene28, auxin repressed-like protein ARP1, gibberellin receptor protein GID1 and auxin-induced protein X10A are involved in both stages mentioned above. In addition to its function in the differentiation and development of the stamens, the gibberellin signaling pathway also functions in embryo sac development for the instaminate flower. The auxin signaling pathway also participates in both stamen development and embryo sac development.
Our transcriptome data provide a comprehensive gene expression profile for flower sex differentiation in Jatropha curcas, as well as new clues and information for further study in this field.
PMCID: PMC4746058  PMID: 26848843
22.  Arabidopsis and Tobacco SUPERMAN regulate hormone signalling and mediate cell proliferation and differentiation 
Journal of Experimental Botany  2010;62(3):949-961.
Arabidopsis thaliana SUPERMAN (SUP) plays an important role during flower development by maintaining the boundary between stamens and carpels in the inner two whorls. It was proposed that SUP maintains this boundary by regulating cell proliferation in both whorls, as loss-of-function superman mutants produce more stamens at the expense of carpels. However, the cellular mechanism that underlies SUP function remains unknown. Here Arabidopsis or tobacco (Nicotiana tabacum) SUP was overexpressed in tobacco plants to substantiate SUP's role as a regulator of cell proliferation and boundary definition and provide evidence that its biological role may be mediated via hormonal changes. It was found that moderate levels of SUP stimulated cell growth and proliferation, whereas high levels were inhibitory. SUP stimulated auxin- and cytokinin-regulated processes, and cells overexpressing SUP displayed reduced hormone dependency for proliferation and regeneration into plants. SUP also induced proliferation of female traits in the second and third flower whorls and promoted differentiation of petaloid properties in sepals, further supporting a role for SUP as a boundary regulator. Moreover, cytokinin suppressed stamen development and promoted differentiation of carpeloid tissues, suggesting that SUP may regulate male and female development via its effect on cytokinin signalling. Taken together, these observations suggest a model whereby the effect of SUP on cell growth and proliferation involves the modulation of auxin- and cytokinin-regulated processes. Furthermore, differential SUP expression or different sensitivities of different cell types to SUP may determine whether SUP stimulates or suppresses their proliferation.
PMCID: PMC3022392  PMID: 20980362
Auxin; cadastral genes; cell proliferation; cytokinin; flower development; SUPERMAN
23.  Transcriptional and hormonal regulation of petal and stamen development by STAMENLESS, the tomato (Solanum lycopersicum L.) orthologue to the B-class APETALA3 gene 
Journal of Experimental Botany  2014;65(9):2243-2256.
Characterization of stamenless mutants reveals that petal and stamen identity in tomato depends on gene–hormone interactions, as mediated by the tomato APETALA3 orthologue STAMENLESS gene (SL, syn. TAP3, SlDEF, LeAP3).
Four B-class MADS box genes specify petal and stamen organ identities in tomato. Several homeotic mutants affected in petal and stamen development were described in this model species, although the causal mutations have not been identified for most of them. In this study we characterized a strong stamenless mutant in the tomato Primabel cultivar (sl-Pr), which exhibited homeotic conversion of petals into sepals and stamens into carpels and we compared it with the stamenless mutant in the LA0269 accession (sl-LA0269). Genetic complementation analysis proved that both sl mutants were allelic. Sequencing revealed point mutations in the coding sequence of the Tomato APETALA3 (TAP3) gene of the sl-Pr genome, which lead to a truncated protein, whereas a chromosomal rearrangement in the TAP3 promoter was detected in the sl-LA0269 allele. Moreover, the floral phenotype of TAP3 antisense plants exhibited identical homeotic changes to sl mutants. These results demonstrate that SL is the tomato AP3 orthologue and that the mutant phenotype correlated to the SL silencing level. Expression analyses showed that the sl-Pr mutation does not affect the expression of other tomato B-class genes, although SL may repress the A-class gene MACROCALYX. A partial reversion of the sl phenotype by gibberellins, gene expression analysis, and hormone quantification in sl flowers revealed a role of phytohormones in flower development downstream of the SL gene. Together, our results indicated that petal and stamen identity in tomato depends on gene–hormone interactions, as mediated by the SL gene.
PMCID: PMC4036497  PMID: 24659487
APETALA3; B-class gene; flower morphogenesis; hormone regulation; Solanum lycopersicum; STAMENLESS; tomato.
24.  Emergence and patterning of the five cell types of the Zea mays anther locule 
Developmental biology  2010;350(1):32-49.
One fundamental difference between plants and animals is the existence of a germ-line in animals and its absence in plants. In flowering plants the sexual organs (stamens and carpels) are composed almost entirely of somatic cells, a small subset of which switch to meiosis, however, the mechanism of meiotic cell fate acquisition is a long-standing botanical mystery. In the maize (Zea mays) anther microsporangium the somatic tissues consist of four concentric cell layers which surround and support reproductive cells as they progress through meiosis and pollen maturation. Male sterility, defined as the absence of viable pollen, is a common phenotype in flowering plants, and many male sterile mutants have defects in somatic and reproductive cell fate acquisition. However, without a robust model of anther cell fate acquisition based on careful observation of wild type anther ontogeny, interpretation of cell fate mutants is limited. To address this, the pattern of cell proliferation, expansion, and differentiation was tracked in three dimensions over thirty days of wild type (W23) anther development, using anthers stained with propidium iodide (PI) and/or 5-ethynyl-2′-deoxyuridine (EdU) (S-phase label) and imaged by confocal microscopy. The pervading lineage model of anther development claims that new cell layers are generated by coordinated, oriented cell divisions in transient precursor cell types. In reconstructing anther cell division patterns, however, we can only confirm this for the origin of the middle layer (ml) and tapetum, while young anther development appears more complex. We find that each anther cell type undergoes a burst of cell division after specification with a characteristic pattern of both cell expansion and division. Comparisons between two inbreds lines and between ab- and adaxial anther florets indicated near identity: anther development is highly canalized and synchronized. Three classical models of plant organ development are tested and ruled out; however, local clustering of developmental events was identified for several processes, including the first evidence for a direct relationship between the development of ml and tapetal cells. We speculate that small groups of ml and tapetum cells function as a developmental unit dedicated to the development of a single pollen grain.
PMCID: PMC3024885  PMID: 21070762
25.  Distinct double flower varieties in Camellia japonica exhibit both expansion and contraction of C-class gene expression 
BMC Plant Biology  2014;14:288.
Double flower domestication is of great value in ornamental plants and presents an excellent system to study the mechanism of morphological alterations by human selection. The classic ABC model provides a genetic framework underlying the control of floral organ identity and organogenesis from which key regulators have been identified and evaluated in many plant species. Recent molecular studies have underscored the importance of C-class homeotic genes, whose functional attenuation contributed to the floral diversity in various species. Cultivated Camellia japonica L. possesses several types of double flowers, however the molecular mechanism underlying their floral morphological diversification remains unclear.
In this study, we cloned the C-class orthologous gene CjAG in C. japonica. We analyzed the expression patterns of CjAG in wild C. japonica, and performed ectopic expression in Arabidopsis. These results revealed that CjAG shared conserved C-class function that controls stamen and carpel development. Further we analyzed the expression pattern of CjAG in two different C. japonica double-flower varieties, ‘Shibaxueshi’ and ‘Jinpanlizhi’, and showed that expression of CjAG was highly contracted in ‘Shibaxueshi’ but expanded in inner petals of ‘Jinpanlizhi’. Moreover, detailed expression analyses of B- and C-class genes have uncovered differential patterns of B-class genes in the inner organs of ‘Jinpanlizhi’.
These results demonstrated that the contraction and expansion of CjAG expression were associated with the formation of different types of double flowers. Our studies have manifested two different trajectories of double flower domestication regarding the C-class gene expression in C. japonica.
Electronic supplementary material
The online version of this article (doi:10.1186/s12870-014-0288-1) contains supplementary material, which is available to authorized users.
PMCID: PMC4219040  PMID: 25344122
Double flower; AGAMOUS; Camellia; Domestication

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