Control of Reproductive Floral Organ Identity Specification inArabidopsisby the C Function Regulator AGAMOUS  

Abstract

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 ...

Floral Organogenesis: When Knowing Your ABCs Is Not Enough

“…That this idea is at least in part correct for the floral organ identity factors is suggested by the expression of the corresponding genes in floral organs throughout most of their morphogenesis (Ó'Maoiléidigh et al, 2014a(Ó'Maoiléidigh et al, , 2014b. Also, the results of perturbation experiments, in which the floral organ identity genes were specifically disrupted or activated at different floral stages, showed that these master regulators have crucial functions in processes that take place during intermediate and late stages of flower development (Ito et al, 2007;Wuest et al, 2012;Ó'Maoiléidigh et al, 2013). However, the now prevailing view is that they largely act by controlling the expression of other genes with regulatory functions.…”

“…In particular, it is currently not known how the MADS protein complexes act at the mechanistic level. The different floral organ identity factors have similar albeit not identical DNA binding specificities , and the results of genomewide localization studies (Kaufmann et al, 2009(Kaufmann et al, , 2010Wuest et al, 2012;Ó'Maoiléidigh et al, 2013;Pajoro et al, 2014) showed that their global binding patterns exhibit large overlaps even in cases where two factors are not part of the same complex. At the same time, the sets of bona fide target genes, i.e.…”

“…genes that are bound and respond to a perturbation of the different floral organ identity factors, are largely distinct (Yan et al, 2016). Furthermore, the expression of the majority of genes bound by the floral organ identity factors is not, or only slightly, altered upon binding by the MADS protein complexes (Kaufmann et al, 2010;Wuest et al, 2012;Ó'Maoiléidigh et al, 2013). Thus, it appears possible that a large number of their binding sites in the genome are nonfunctional at least in the context of floral organ identity specification (i.e.…”

PIFs: Systems Integrators in Plant Development

“…In addition to the described binding by BZR1 , BRs might also target PIF5 through direct binding by BES1 . Intriguingly, several transcription factors involved in the regulation of flowering (AP1, SVP, LFY, AG, and SEP3) have also been identified to bind PIFs (Kaufmann et al, 2009(Kaufmann et al, , 2010Moyroud et al, 2011;Tao et al, 2012;Gregis et al, 2013;ÓMaoiléidigh et al, 2013), suggesting a direct link to the reported flowering phenotype of pif mutants (Brock et al, 2010;Nozue et al, 2011;Kumar et al, 2012). Finally, binding by REV and AGL15 (Zheng et al, 2009;Brandt et al, 2012) suggests that some of the PIFs might be involved in leaf patterning or embryogenesis, a possibility that needs to be explored.…”

Genome-Wide Targets Regulated by the OsMADS1 Transcription Factor Reveals Its DNA Recognition Properties

“…Studies on the genome-wide binding of Arabidopsis MADS-domain proteins identify mechanisms underlying their role during flower development (Kaufmann et al, 2009Immink et al, 2012;Deng et al, 2011;Zheng et al, 2009;Wuest et al, 2012;Ó'Maoiléidigh et al, 2013;Gregis et al, 2013). These studies showed them to bind a multitude of downstream target genes and regulate their expression.…”