Arabidopsis (Arabidopsis thaliana) floral meristems terminate after the carpel primordia arise. This is achieved through the temporal repression of WUSCHEL (WUS), which is essential for stem cell maintenance. At floral stage 6, WUS is repressed by KNUCKLES (KNU), a repressor directly activated by AGAMOUS. KNU was suggested to repress WUS through histone deacetylation; however, how the changes in the chromatin state of WUS are initiated and maintained to terminate the floral meristem remains elusive. Here, we show that KNU integrates initial transcriptional repression with polycomb-mediated stable silencing of WUS. After KNU is induced, it binds to the WUS promoter and causes eviction of SPLAYED, which is a known activator of WUS and can oppose polycomb repression. KNU also physically interacts with FERTILIZATION-INDEPENDENT ENDOSPERM, a key polycomb repressive complex2 component, and mediates the subsequent deposition of the repressive histone H3 lysine 27 trimethylation for stable silencing of WUS. This multi-step silencing of WUS leads to the termination of floral stem cells, ensuring proper carpel development. Thus, our work describes a detailed mechanism for heritable floral stem cell termination in a precise spatiotemporal manner.

Floral organs are properly developed on the basis of timed floral meristem (FM) termination in Arabidopsis. In this process, two known regulatory pathways are involved. The WUSCHEL (WUS)-CLAVATA3 (CLV3) feedback loop is vital for the spatial establishment and maintenance of the FM, while AGAMOUS (AG)-WUS transcriptional cascades temporally repress FM. At stage 6 of flower development, a C2H2-type zinc finger repressor that is a target of AG, KNUCKLES (KNU), directly represses the stem cell identity gene WUS in the organizing center for FM termination. However, how the robust FM activity is fully quenched within a limited time frame to secure carpel development is not fully understood. Here, we demonstrate that KNU directly binds to the CLV1 locus and the cis-regulatory element on CLV3 promoter and represses their expression during FM determinacy control. Furthermore, KNU physically interacts with WUS, and this interaction inhibits WUS from sustaining CLV3 in the central zone. The KNU–WUS interaction also interrupts the formation of WUS homodimers and WUS–HAIRYMERISTEM 1 heterodimers, both of which are required for FM maintenance. Overall, our findings describe a regulatory framework in which KNU plays a position-specific multifunctional role for the tightly controlled FM determinacy.

In Arabidopsis, the floral meristem is essential for the production of floral organs. The floral meristem is initially maintained to contribute cells for floral organ formation. However, this stem cell activity needs be completely terminated at a certain floral developmental stage to ensure the proper development of floral reproductive organs. Here, we have reviewed recent findings on the complex regulation of floral meristem activities, which involve signaling cascades, transcriptional regulation, epigenetic mechanisms and hormonal control for floral meristem determinacy in Arabidopsis.

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