Developmental regulation of the floral meristem ensures that plants of the same species have similarly sized flowers with a fixed number of floral organs. The maintenance of stem cells in the floral meristem is terminated after the production of a fixed number of floral organ primordia. Precise repression of the Arabidopsis thaliana homeobox gene WUSCHEL (WUS) by the floral homeotic protein AGAMOUS (AG) plays a major part in this process. Here we show that KNUCKLES (KNU) mediates the repression of WUS in floral meristem determinacy control. AG directly induces the transcription of KNU, which encodes a C2H2-type zinc finger protein with a conserved transcriptional repression motif. In turn, KNU represses WUS transcription to abolish stem cell activity. We also show that the timing of KNU induction is key in balancing proliferation and differentiation in flower development. Delayed KNU expression results in an indeterminate meristem, whereas ectopic KNU expression prematurely terminates the floral meristem. Furthermore, KNU induction by AG is preceded by changes in repressive histone modification at the KNU locus, which occurs in an AG-dependent manner. This study provides a mechanistic link between transcriptional feedback and epigenetic regulation in plant stem cell proliferation.

A Matter of Timing: Plants flower only when their developmental programs give the go-ahead; otherwise floral genes remain repressed. Sun et al. ( 10.1126/science.1248559 ; see the Perspective by Zhang ) analyzed the regulatory program that controls expression of the transcription factor KNUCKLES (KNU), which is required in the control of floral genes. KNU expression was silenced by the presence of Polycomb group (PcG) proteins. The floral homeotic protein AGAMOUS competed for control of KNU and activated its expression, but with a 2-day lag time. Thus, eviction of PcG by activating DNA binding proteins can insert a lag time before a switch in gene expression takes place.

Flower development begins as floral meristems arise in succession on the flank of the inflorescence meristem. Floral meristem identity genes LEAFY (LFY) and APETALA1 (AP1) promote establishment and maintenance of floral identity in newly formed floral primordia^{1,2,3,4,5,6,7,8,9}. Without their activity, the floral primordia develop with inflorescence characteristics. The underlying molecular-genetic mechanism is unknown. Here we show that these phenotypes are due in large part to the ectopic expression of AGAMOUS-LIKE 24 (AGL24), a central regulator of floral meristem identity. We present evidence that AGL24 is an early target of transcriptional repression by LFY and AP1. Without such repression, continued AGL24 expression in floral meristems is sufficient to cause floral reversion regardless of the activation of floral organ identity genes. This indicates that LFY and AP1 promote floral development not only by positively regulating genes activated in flower development, but also by repressing AGL24, a promoter of inflorescence fate.

The Arabidopsis thaliana floral homeotic gene AGAMOUS (AG) plays a central role in reproductive organ (stamen and carpel) development. AG RNA is expressed in the center of floral primordia from a time prior to the initiation of stamen and carpel primordia until late in flower development. While early AG expression acts in specification of stamens and carpels, the role, if any, of continued AG expression in later flower development is unknown. To examine the timing of AG action and its possible late-stage functions, we performed a series of time-course experiments using a transgenic line with inducible AG activity in an ag homozygous mutant background. We show that AG controls late-stage stamen development, including anther morphogenesis and dehiscence, as well as filament formation and elongation. We further show that AG coordinates late stamen maturation by controlling a biosynthetic gene of the lipid-derived phytohormone jasmonic acid (JA). Expression analysis and in vivo binding of AG indicate that AG directly regulates the transcription of a catalytic enzyme of JA, DEFECTIVE IN ANTHER DEHISCENCE1. Our results indicate that stamen identity and differentiation control by AG is achieved by the regulation of different transcriptional cascades in different floral stages, with organ specification induced early, followed by phytohormone biosynthesis to coordinate stamen maturation.