Tracing the Evolution of the Floral Homeotic B- and C-Function Genes through Genome Synteny

The evolution of the floral homeotic genes has been characterized using phylogenetic and functional studies. It is possible to enhance these studies by comparing gene content and order between species to determine the evolutionary history of the regulatory genes. Here, we use a synteny-based approach to trace the evolution of the floral B- and C-function genes that are required for specification of the reproductive organs. Consistent with previous phylogenetic studies, we show that the euAP3–TM6 split occurred after the monocots and dicots diverged. The Arabidopsis TM6 and papaya euAP3 genes are absent from the respective genomes, and we have detected loci from which these genes were lost. These data indicate that either the TM6 or the euAP3 lineage genes can be lost without detriment to flower development. In contrast, PI is essential for male reproductive organ development; yet, contrary to predictions, complex genomic rearrangements have resulted in almost complete breakdown of synteny at the PI locus. In addition to showing the evolution of B-function genes through the prediction of ancestral loci, similar reconstructions reveal the origins of the C-function AG and PLE lineages in dicots, and show the shared ancestry with the monocot C-function genes. During our studies, we found that transposable elements (TEs) present in sequenced Antirrhinum genomic clones limited comparative studies. A pilot survey of the Antirrhinum data revealed that gene-rich regions contain an unusually high degree of TEs of very varied types, which will be an important consideration for future genome sequencing efforts

Conservation versus divergence in LEAFY and APETALA functions between Arabidopsis thaliana and Cardamine hirsuta

International audienceA conserved genetic toolkit underlies the development of diverse floral forms among angiosperms. However, the degree of conservation vs divergence in the configuration of these gene regulatory networks is less clear. We addressed this question in a parallel genetic study between the closely related species Arabidopsis thaliana and Cardamine hirsuta. We identified leafy (lfy) and apetala1 (ap1) alleles in a mutant screen for floral regulators in C. hirsuta. C. hirsuta lfy mutants showed a complete homeotic conversion of flowers to leafy shoots, mimicking lfy ap1 double mutants in A. thaliana. Through genetic and molecular experiments, we showed that AP1 activation is fully dependent on LFY in C. hirsuta, by contrast to A. thaliana. Additionally, we found that LFY influences heteroblasty in C. hirsuta, such that loss or gain of LFY function affects its progression. Overexpression of UNUSUAL FLORAL ORGANS also alters C. hirsuta leaf shape in an LFY-dependent manner. We found that LFY and AP1 are conserved floral regulators that act nonredundantly in C. hirsuta, such that LFY has more obvious roles in floral and leaf development in C. hirsuta than in A. thaliana

An everlasting pioneer: the story of Antirrhinum research

Despite the tremendous success of Arabidopsis thaliana, no single model can represent the vast range of form that is seen in the ~250,000 existing species of flowering plants (angiosperms). Here, we consider the history and future of an alternative angiosperm model — the snapdragon Antirrhinum majus. We ask what made Antirrhinum attractive to the earliest students of variation and inheritance, and how its use led to landmark advances in plant genetics and to our present understanding of plant development. Finally, we show how the wide diversity of Antirrhinum species, combined with classical and molecular genetics — the two traditional strengths of Antirrhinum — provide an opportunity for developmental, evolutionary and ecological approaches. These factors make A. majus an ideal comparative angiosperm

Developmental Robustness by Obligate Interaction of Class B Floral Homeotic Genes and Proteins

DEF-like and GLO-like class B floral homeotic genes encode closely related MADS-domain transcription factors that act as developmental switches involved in specifying the identity of petals and stamens during flower development. Class B gene function requires transcriptional upregulation by an autoregulatory loop that depends on obligate heterodimerization of DEF-like and GLO-like proteins. Because switch-like behavior of gene expression can be displayed by single genes already, the functional relevance of this complex circuitry has remained enigmatic. On the basis of a stochastic in silico model of class B gene and protein interactions, we suggest that obligate heterodimerization of class B floral homeotic proteins is not simply the result of neutral drift but enhanced the robustness of cell-fate organ identity decisions in the presence of stochastic noise. This finding strongly corroborates the view that the appearance of this regulatory mechanism during angiosperm phylogeny led to a canalization of flower development and evolution

The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro

The organs of a eudicot flower are specified by four functional classes, termed class A, B, C and E, of MADS domain transcription factors. The combinatorial formation of tetrameric complexes, so called ‘floral quartets’, between these classes is widely believed to represent the molecular basis of floral organ identity specification. As constituents of all complexes, the class E floral homeotic proteins are thought to be of critical relevance for the formation of floral quartets. However, experimental support for tetrameric complex formation remains scarce. Here we provide physico-chemical evidence that in vitro homotetramers of the class E floral homeotic protein SEPALLATA3 from Arabidopsis thaliana bind cooperatively to two sequence elements termed ‘CArG boxes’ in a phase-dependent manner involving DNA looping. We further show that the N-terminal part of SEPALLATA3 lacking K3, a subdomain of the protein–protein interactions mediating K domain, and the C-terminal domain, is sufficient for protein dimerization, but not for tetramer formation and cooperative DNA binding. We hypothesize that the capacity of class E MADS domain proteins to form tetrameric complexes contributes significantly to the formation of floral quartets. Our findings further suggest that the spacing and phasing of CArG boxes are important parameters in the molecular mechanism by which floral homeotic proteins achieve target gene specificity

Cryptic Variation between Species and the Basis of Hybrid Performance

Studies on natural variation in gene expression and its phenotypic effects provide fresh insights into the origins of vigour and sterility in species hybrids