How different organs are formed from small sets of undifferentiated precursor cells is a key question in developmental biology. To understand the molecular mechanisms underlying organ specification in plants, we studied the function of the homeotic selector genes APETALA3 (AP3) and PISTILLATA (PI), which control the formation of petals and stamens during Arabidopsis flower development. To this end, we characterized the activities of the transcription factors that AP3 and PI encode throughout flower development by using perturbation assays as well as transcript profiling and genomewide localization studies, in combination with a floral induction system that allows a stage-specific analysis of flower development by genomic technologies. We discovered considerable spatial and temporal differences in the requirement for AP3/PI activity during flower formation and show that they control different sets of genes at distinct phases of flower development. The genomewide identification of target genes revealed that AP3/PI act as bifunctional transcription factors: they activate genes involved in the control of numerous developmental processes required for organogenesis and repress key regulators of carpel formation. Our results imply considerable changes in the composition and topology of the gene network controlled by AP3/PI during the course of flower development. We discuss our results in light of a model for the mechanism underlying sex-determination in seed plants, in which AP3/PI orthologues might act as a switch between the activation of male and the repression of female development.F lowers are typically composed of four organ types, which are disposed in four floral whorls. From the outside of the flower to the center, they are sepals, petals, stamens, and carpels (the subunits of the gynoecium). The developmental fate of these different types of organs is specified by a small number of floral organ identity genes. The pivotal role of these genes was uncovered through the analysis of mutants that form flowers with homeotic transformations, i.e., the replacement of one type of organ with another (1-4). Based on the morphological defects of the individual mutants and their genetic interactions, it was proposed that the floral organ identity genes act in a combinatorial manner and have distinct functions during flower development, with the so-called A function genes being required for the formation of sepals and petals, B function genes for petal and stamen development, and C function genes for the formation of stamens and carpels. This well-established ABC model of floral organ identity specification (5) has provided, since its introduction more than 20 y ago, an invaluable framework for the analysis of the genetic mechanisms underlying the formation and evolution of flowers.Molecular characterization of the floral organ identity genes in different species revealed that they encode transcription factors and belong, with few exceptions, to the family of MADS domain proteins (1-3). The floral organ identity factors w...
BackgroundDevelopment of eukaryotic organisms is controlled by transcription factors that trigger specific and global changes in gene expression programs. In plants, MADS-domain transcription factors act as master regulators of developmental switches and organ specification. However, the mechanisms by which these factors dynamically regulate the expression of their target genes at different developmental stages are still poorly understood.ResultsWe characterized the relationship of chromatin accessibility, gene expression, and DNA binding of two MADS-domain proteins at different stages of Arabidopsis flower development. Dynamic changes in APETALA1 and SEPALLATA3 DNA binding correlated with changes in gene expression, and many of the target genes could be associated with the developmental stage in which they are transcriptionally controlled. We also observe dynamic changes in chromatin accessibility during flower development. Remarkably, DNA binding of APETALA1 and SEPALLATA3 is largely independent of the accessibility status of their binding regions and it can precede increases in DNA accessibility. These results suggest that APETALA1 and SEPALLATA3 may modulate chromatin accessibility, thereby facilitating access of other transcriptional regulators to their target genes.ConclusionsOur findings indicate that different homeotic factors regulate partly overlapping, yet also distinctive sets of target genes in a partly stage-specific fashion. By combining the information from DNA-binding and gene expression data, we are able to propose models of stage-specific regulatory interactions, thereby addressing dynamics of regulatory networks throughout flower development. Furthermore, MADS-domain TFs may regulate gene expression by alternative strategies, one of which is modulation of chromatin accessibility.
The floral organ identity factor AGAMOUS (AG) is a key regulator of Arabidopsis thaliana flower development, where it is involved in the formation of the reproductive floral organs as well as in the control of meristem determinacy. To obtain insights into how AG specifies organ fate, we determined the genes and processes acting downstream of this C function regulator during early flower development and distinguished between direct and indirect effects. To this end, we combined genome-wide localization studies, gene perturbation experiments, and computational analyses. Our results demonstrate that AG controls flower development to a large extent by controlling the expression of other genes with regulatory functions, which are involved in mediating a plethora of different developmental processes. One aspect of this function is the suppression of the leaf development program in emerging floral primordia. Using trichome initiation as an example, we demonstrate that AG inhibits an important aspect of leaf development through the direct control of key regulatory genes. A comparison of the gene expression programs controlled by AG and the B function regulators APETALA3 and PISTILLATA, respectively, showed that while they control many developmental processes in conjunction, they also have marked antagonistic, as well as independent activities. INTRODUCTIONHow different types of organs are formed from undifferentiated stem cells is a central question in biology. It is known that in both plants and animals, organogenesis is controlled to a large extent by master regulatory genes, which typically encode transcription factors. While it is currently not well understood how these regulators act at the molecular level, the recent development of experimental approaches that allow the characterization of protein-DNA interactions and transcriptional profiles on a genome-wide scale has led to detailed insights into the function of some of these transcription factors (Wellmer and Riechmann, 2005;Hueber and Lohmann, 2008).In flowering plants, the different types of floral organs (i.e., sepals, petals, stamens, and carpels) are specified by the activities of a small set of master regulators, termed floral organ identity genes Coen and Meyerowitz, 1991). The pivotal role of these genes in flower development was uncovered through the identification of mutants that exhibit homeotic transformations (i.e., the replacement of one organ type by another) . Based on the phenotypes of these mutants, it was proposed that the floral organ identity genes control organ fate in a combinatorial manner (Coen and Meyerowitz, 1991). According to this socalled ABC model, sepals are specified by A function genes, petals by a combination of A and B function activities, stamens by B and C function genes, and carpels by C function gene activity alone. The molecular characterization of the genes affected in floral homeotic mutants in different species showed that they encode transcription factors and belong, with few exceptions, to the family of MADS domain ...
16I.16II.17III.18IV.19V.21VI.23VII.26VIII.2627References27 Summary The formation of flowers is one of the main models for studying the regulatory mechanisms that underlie plant development and evolution. Over the past three decades, extensive genetic and molecular analyses have led to the identification of a large number of key floral regulators and to detailed insights into how they control flower morphogenesis. In recent years, genome‐wide approaches have been applied to obtaining a global view of the gene regulatory networks underlying flower formation. Furthermore, mathematical models have been developed that can simulate certain aspects of this process and drive further experimentation. Here, we review some of the main findings made in the field of Arabidopsis thaliana flower development, with an emphasis on recent advances. In particular, we discuss the activities of the floral organ identity factors, which are pivotal for the specification of the different types of floral organs, and explore the experimental avenues that may elucidate the molecular mechanisms and gene expression programs through which these master regulators of flower development act.
The transcription factors LEAFY (LFY) and APETALA1 (AP1), together with the AP1 paralog CAULIFLOWER (CAL), control the onset of flower development in a partially redundant manner. This redundancy is thought to be mediated, at least in part, through the regulation of a shared set of target genes. However, whether these genes are independently or cooperatively regulated by LFY and AP1/CAL is currently unknown. To better understand the regulatory relationship between LFY and AP1/CAL and to obtain deeper insights into the control of floral initiation, we monitored the activity of LFY in the absence of AP1/CAL function. We found that the regulation of several known LFY target genes is unaffected by AP1/CAL perturbation, while others appear to require AP1/CAL activity. Furthermore, we obtained evidence that LFY and AP1/CAL control the expression of some genes in an antagonistic manner. Notably, these include key regulators of floral initiation such as (), which had been previously reported to be directly repressed by both LFY and AP1. We show here that expression is suppressed by AP1 but promoted by LFY. We further demonstrate that LFY has an inhibitory effect on flower formation in the absence of AP1/CAL activity. We propose that LFY and AP1/CAL act as part of an incoherent feed-forward loop, a network motif where two interconnected pathways or transcription factors act in opposite directions on a target gene, to control the establishment of a stable developmental program for the formation of flowers.
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