Heterotopic expression of class B floral homeotic genes supports a modified ABC model for tulip (Tulipa gesneriana)

In higher eudicotyledonous angiosperms the floral organs are typically arranged in four different whorls, containing sepals, petals, stamens and carpels. According to the ABC model, the identity of these organs is specified by floral homeotic genes of class A, A+B, B+C and C, respectively. In contrast to the sepal and petal whorls of eudicots, the perianths of many plants from the Liliaceae family have two outer whorls of almost identical petaloid organs, called tepals. To explain the Liliaceae flower morphology, van Tunen et al. (1993) proposed a modified ABC model, exemplified with tulip. According to this model, class B genes are not only expressed in whorls 2 and 3, but also in whorl 1. Thus the organs of both whorls 1 and 2 express class A plus class B genes and, therefore, get the same petaloid identity. To test this modified ABC model we have cloned and characterized putative class B genes from tulip. Two DEF- and one GLO-like gene were identified, named TGDEFA, TGDEFB and TGGLO. Northern hybridization analysis showed that all of these genes are expressed in whorls 1, 2 and 3 (outer and inner tepals and stamens), thus corroborating the modified ABC model. In addition, these experiments demonstrated that TGGLO is also weakly expressed in carpels, leaves, stems and bracts. Gel retardation assays revealed that TGGLO alone binds to DNA as a homodimer. In contrast, TGDEFA and TGDEFB cannot homodimerize, but make heterodimers with PI. Homodimerization of GLO-like protein has also been reported for lily, suggesting that this phenomenon is conserved within Liliaceae plants or even monocot species.these authors contributed equally to this work     

花器官发育的分子机制研究进展

经典的ABC模型成功地解释了模式植物拟南芥和金鱼草因同源异型基因突变而引起的植物花器官的变异。随后,大量花器官特征基因和新突变体的研究不断完善和发展了ABC模型。该文综述了近年来花器官发育分子模型及花器官同源基因的调控机理等方面的最新研究成果,并对未来的研究方向进行了展望,以期为深入了解花发育的分子机理和遗传机制奠定基础。     

Expression of floral MADS-box genes in basal angiosperms: implications for the evolution of floral regulators

The ABC model of floral organ identity is based on studies of Arabidopsis and Antirrhinum, both of which are highly derived eudicots. Most of the genes required for the ABC functions in Arabidopsis and Antirrhinum are members of the MADS-box gene family, and their orthologs are present in all major angiosperm lineages. Although the eudicots comprise 75% of all angiosperms, most of the diversity in arrangement and number of floral parts is actually found among basal angiosperm lineages, for which little is known about the genes that control floral development. To investigate the conservation and divergence of expression patterns of floral MADS-box genes in basal angiosperms relative to eudicot model systems, we isolated several floral MADS-box genes and examined their expression patterns in representative species, including Amborella (Amborellaceae), Nuphar (Nymphaeaceae) and Illicium (Austrobaileyales), the successive sister groups to all other extant angiosperms, plus Magnolia and Asimina, members of the large magnoliid clade. Our results from multiple methods (relative-quantitative RT-PCR, real-time PCR and RNA in situ hybridization) revealed that expression patterns of floral MADS-box genes in basal angiosperms are broader than those of their counterparts in eudicots and monocots. In particular, (i) AP1 homologs are generally expressed in all floral organs and leaves, (ii) AP3/PI homologs are generally expressed in all floral organs and (iii) AG homologs are expressed in stamens and carpels of most basal angiosperms, in agreement with the expectations of the ABC model; however, an AG homolog is also expressed in the tepals of Illicium. The broader range of strong expression of AP3/PI homologs is inferred to be the ancestral pattern for all angiosperms and is also consistent with the gradual morphological intergradations often observed between adjacent floral organs in basal angiosperms.     

The ABC model and its applicability to basal angiosperms

BACKGROUND: Although the flower is the central feature of the angiosperms, little is known of its origin and subsequent diversification. The ABC model has long been the unifying paradigm for floral developmental genetics, but it is based on phylogenetically derived eudicot models. Synergistic research involving phylogenetics, classical developmental studies, genomics and developmental genetics has afforded valuable new insights into floral evolution in general, and the early flower in particular. SCOPE AND CONCLUSIONS: Genomic studies indicate that basal angiosperms, and by inference the earliest angiosperms, had a rich tool kit of floral genes. Homologues of the ABCE floral organ identity genes are also present in basal angiosperm lineages; however, C-, E- and particularly B-function genes are more broadly expressed in basal lineages. There is no single model of floral organ identity that applies to all angiosperms; there are multiple models that apply depending on the phylogenetic position and floral structure of the group in question. The classic ABC (or ABCE) model may work well for most eudicots. However, modifications are needed for basal eudicots and, the focus of this paper, basal angiosperms. We offer 'fading borders' as a testable hypothesis for the basal-most angiosperms and, by inference, perhaps some of the earliest (now extinct) angiosperms.     

A floral meristem identity gene influences physiological and ecological aspect of floral organogenesis

The architecture of a flower is tightly linked to the way a plant pollinates, making it one of the most physiologically and ecologically important traits of angiosperms. Floral organ development is proposed to be governed by the activity of three different classes of organ identity genes (the ABC model), and the expression of those genes are regulated by a number of meristem identity genes. Here we use a transgenetic strategy to elucidate the role of one floral meristem identify gene,LEAFY (LFY), in the evolution of floral organogenesis of a self pollinatorIdahoa scapigera and a obligatory out-crosserLeavenworthia crassa in the mustard family, Brassicaceae. By introducing theLFY genes from these two types of pollination habit into the genetic model speciesArabidopsis thaliana, we provide evidence that changes inLFY influenced flower architecture probably by controlling the downstream organ identity genes.     

Functional analyses of AGAMOUS family members in Nicotiana benthamiana clarify the evolution of early and late roles of C-function genes in eudicots

The C-function, according to the ABC model of floral organ identity, is required for stamen and carpel development and to provide floral meristem determinacy. Members of the AG lineage of the large MADS box gene family specify the C-function in a broadly conserved manner in angiosperms. In core eudicots, two sub-lineages co-exist, euAG and PLE, which have been extensively characterized in Antirrhinum majus and Arabidopsis thaliana, where strong sub-functionalization has led to highly divergent contributions of the respective paralogs to the C-function. Various scenarios have been proposed to reconstruct the evolutionary history of the euAG and PLE lineages in eudicots, but detailed functional analyses of the roles of these genes in additional representative species to validate evolutionary hypotheses are scarce. Here, we report functional characterization of euAG- and PLE-like genes in Nicotiana benthamiana through expression analyses and phenotypic characterization of the defects caused by their specific down-regulation. We show that both paralogs redundantly contribute to the C-function in this species, providing insights on the likely evolution of these gene lineages following divergence of the major groups within the eudicots (rosids and asterids). Moreover, we have demonstrated a conserved role for the PLE-like genes in controlling fruit dehiscence, which strongly supports the ancestral role of PLE-like genes in late fruit development and suggests a common evolutionary origin of late developmental processes in dry (dehiscent) and fleshy (ripening) fruits.     

Duplication of <Emphasis Type="Italic">AP1</Emphasis> within the <Emphasis Type="Italic">Spinacia oleracea</Emphasis> L. <Emphasis Type="Italic">AP1/FUL</Emphasis> clade is followed by rapid amino acid and regulatory evolution

The AP1/FUL clade of MADS box genes have undergone multiple duplication events among angiosperm species. While initially identified as having floral meristem identity and floral organ identity function in Arabidopsis, the role of AP1 homologs does not appear to be universally conserved even among eudicots. In comparison, the role of FRUITFULL has not been extensively explored in non-model species. We report on the isolation of three AP1/FUL genes from cultivated spinach, Spinacia oleracea L. Two genes, designated SpAPETALA1-1 (SpAP1-1) and SpAPETALA1-2 (SpAP1-2), cluster as paralogous genes within the Caryophyllales AP1 clade. They are highly differentiated in the 3′, carboxyl-end encoding region of the gene following the third amphipathic alpha-helix region, while still retaining some elements of a signature AP1 carboxyl motifs. In situ hybridization studies also demonstrate that the two paralogs have evolved different temporal and spatial expression patterns, and that neither gene is expressed in the developing sepal whorl, suggesting that the AP1 floral organ identity function is not conserved in spinach. The spinach FRUITFULL homolog, SpFRUITFULL (SpFUL), has retained the conserved motif and groups with Caryophyllales FRUITFULL homologs. SpFUL is expressed in leaf as well as in floral tissue, and shows strong expression late in flower development, particularly in the tapetal layer in males, and in the endothecium layer and stigma, in the females. The combined evidence of high rates of non-synonymous substitutions and differential expression patterns supports a scenario in which the AP1 homologs in the spinach AP1/FUL gene family have experienced rapid evolution following duplication. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

The ABCs of flower development: mutational analysis of AP1/FUL‐like genes in rice provides evidence for a homeotic (A)‐function in grasses

The well‐known ABC model describes the combinatorial interaction of homeotic genes in specifying floral organ identities. While the B‐ and C‐functions are highly conserved throughout flowering plants and even in gymnosperms, the A‐function, which specifies the identity of perianth organs (sepals and petals in eudicots), remains controversial. One reason for this is that in most plants that have been investigated thus far, with Arabidopsis being a remarkable exception, one does not find recessive mutants in which the identity of both types of perianth organs is affected. Here we report a comprehensive mutational analysis of all four members of the AP1/FUL‐like subfamily of MADS‐box genes in rice (Oryza sativa). We demonstrate that OsMADS14 and OsMADS15, in addition to their function of specifying meristem identity, are also required to specify palea and lodicule identities. Because these two grass‐specific organs are very likely homologous to sepals and petals of eudicots, respectively, we conclude that there is a floral homeotic (A)‐function in rice as defined previously. Together with other recent findings, our data suggest that AP1/FUL‐like genes were independently recruited to fulfil the (A)‐function in grasses and some eudicots, even though other scenarios cannot be excluded and are discussed.     

Genome analysis of amaranths: Determination of inter- and intra-species variations

Amaranths are an important group of plants and include grain, vegetable and ornamental types. Despite the economic importance of the amaranths, there is very little information available about the extent and nature of genetic diversity present in the genus Amaranthus at molecular level. We now report the randomly amplified polymorphic DNA (RAPD) profiles of different species of Amaranthus as well as different accessions of the species. These RAPD analyses have been carried out using 65 arbitrary sequence decamer primers. From the RAPD data, an UPGMA dendrogram illustrating the inter-as well as intra-species relationships has been computed. The putative hybrid origin of A.dubious from A. hybridus and A. spinosus is also ruled out by the RAPD data. The trends of species relationships amongst the amaranths determined by RAPDs is consistent with their cytogenetic and evolutionary relationships that have already been determined. NBRI Communication No:464 (N.S.).     

The expression of floral organ identity genes in contrasting water lily cultivars

The floral organs of typical eudicots such as Arabidopsis thaliana are arranged in four characteristic whorls, namely the sepal, petal, stamen and carpel, and the “ABC” floral organ identity model has been based on this arrangement. However, the floral organs in most basal angiosperms are spirally arranged with a gradual transition from the inside to outside, and an alternative model referred to as “fading borders” was developed to take account of this. The flower morphology of the water lily was tested against the “fading borders” model by determining the expression profile of the six primary floral organ identity genes AP2, AGL6, AP3, PI, AG and SEP1 in two cultivars showing contrasting floral morphology. In addition, to get accurate floatation of the genes expression level from outer to inner, we divided the floral organs into eight whorls according to morphological features. All these genes were expressed throughout all whorls of the flower, but their expression level changed gradually from the outside of the flower to its inside. This pattern was consistent with the “fading borders” model.     

A gene regulatory network model for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles

Flowers are icons in developmental studies of complex structures. The vast majority of 250,000 angiosperm plant species have flowers with a conserved organ plan bearing sepals, petals, stamens, and carpels in the center. The combinatorial model for the activity of the so-called ABC homeotic floral genes has guided extensive experimental studies in Arabidopsis thaliana and many other plant species. However, a mechanistic and dynamical explanation for the ABC model and prevalence among flowering plants is lacking. Here, we put forward a simple discrete model that postulates logical rules that formally summarize published ABC and non-ABC gene interaction data for Arabidopsis floral organ cell fate determination and integrates this data into a dynamic network model. This model shows that all possible initial conditions converge to few steady gene activity states that match gene expression profiles observed experimentally in primordial floral organ cells of wild-type and mutant plants. Therefore, the network proposed here provides a dynamical explanation for the ABC model and shows that precise signaling pathways are not required to restrain cell types to those found in Arabidopsis, but these are rather determined by the overall gene network dynamics. Furthermore, we performed robustness analyses that clearly show that the cell types recovered depend on the network architecture rather than on specific values of the model's gene interaction parameters. These results support the hypothesis that such a network constitutes a developmental module, and hence provide a possible explanation for the overall conservation of the ABC model and overall floral plan among angiosperms. In addition, we have been able to predict the effects of differences in network architecture between Arabidopsis and Petunia hybrida.     

Organization of the chromosome region harboring a FLORICAULA/LEAFY gene in Liriodendron

FLORICAULA/LEAFY (FLO/LFY) plays an important role in the reproductive transition and controls flower spatial patterning by inducing the expression of the ABC floral organ identity genes. In this study, we sequenced two bacterial artificial chromosomes harboring a FLO/LFY and three other genes from yellow-poplar (Liriodendron tulipifera L.) and compared the gene order in this locus between several species. Besides the conserved terminal domains, key residues involved in interactions with DNA bases, backbone, and in dimerization were also conserved in the yellow-poplar FLO/LFY. Phylogenetic analysis of the FLO/LFY amino acid sequences placed yellow-poplar closer to eudicots than to monocotyledonous species. We found that gene content and order in this region of the yellow-poplar genome was more similar to corresponding regions in Vitis vinifera L., Carica papaya L., Populus trichocarpa Torr. & Gray, and Ricinus communis L., regardless of the evolutionary relationship. In addition, evidence for transposition, large insertions, and duplications were found, suggesting multiple and complex mechanisms of basal angiosperm genome evolution.     

花同源异型MADS-box 基因在被子植物中的功能保守性和多样性

MADS-box基因家族成员作为转录调控因子在被子植物花发育调控中发挥关键作用。本文以模式植物拟南芥(Arabidopsis thaliana) 和水稻 (Oryza sativa)为例, 综述了近10年来对被子植物(又称有花植物)两大主要类群——核心真 双子叶植物和单子叶植物花同源异型MADS-box基因的研究成果, 分析MADS-box基因在被子植物中的功能保守性和多样性,同时探讨双子叶植物花发育的ABCDE模型在多大程度上适用于单子叶植物。     

The floral genome: an evolutionary history of gene duplication and shifting patterns of gene expression

Through multifaceted genome-scale research involving phylogenomics, targeted gene surveys, and gene expression analyses in diverse basal lineages of angiosperms, our studies provide insights into the most recent common ancestor of all extant flowering plants. MADS-box gene duplications have played an important role in the origin and diversification of angiosperms. Furthermore, early angiosperms possessed a diverse tool kit of floral genes and exhibited developmental 'flexibility', with broader patterns of expression of key floral organ identity genes than are found in eudicots. In particular, homologs of B-function MADS-box genes are more broadly expressed across the floral meristem in basal lineages. These results prompted formulation of the 'fading borders' model, which states that the gradual transitions in floral organ morphology observed in some basal angiosperms (e.g. Amborella) result from a gradient in the level of expression of floral organ identity genes across the developing floral meristem.