LEAFY and APETALA1 down-regulate ZINC FINGER PROTEIN 1 and 8 to release their repression on class B and C floral homeotic genes

Abstract

Organ initiation from the shoot apical meristem first gives rise to leaves during vegetative development and then flowers during reproductive development. LEAFY ( LFY ) is activated after floral induction and together with other factors promotes the floral program. LFY functions redundantly with APETALA1 (AP1) to activate the class B genes APETALA3 ( AP3 ) and PISTILLATA ( PI ), the class C gene AGAMOUS ( AG ), and the class E gene SEPALLATA3 , which leads to the specification of stamens and carpels, the reproductive organs of flowers. Molecular and genetic networks that control the activation of AP3, PI, and AG in flowers have been well studied; however, much less is known about how these genes are repressed in leaves and how their repression is lifted in flowers. Here, we showed that two genes encoding Arabidopsis C2H2 ZINC FINGER PROTEIN (ZFP) transcription factors, ZP1 and ZFP8, act redundantly to directly repress AP3, PI, and AG in leaves. After LFY and AP1 are activated in floral meristems, they down-regulate ZP1 and ZFP8 directly to lift the repression on AP3, PI, and AG . Our results reveal a mechanism for how floral homeotic genes are repressed and derepressed before and after floral induction.

Reflections on the ABC model of flower development

“…ABC genes must also keep quiet during the vegetative phase at the risk of interfering with correct leaf development; this is not simply due to the absence of LFY but also necessitates active silencing of floral homeotic genes ( Goodrich et al 1997 ). Recent studies have started to identify specific factors involved in recruiting polycomb complexes to those loci: for instance, 2 Zinc Fingers were shown to recruit PRC2 to induce heterochromatin formation at APETALA1 , APETALA3 , and AGAMOUS in Arabidopsis ( Hu et al 2023 ). Those factors are repressed by LFY and APETALA1, allowing release of vegetative inhibition once floral induction is set in motion.…”

Old school, new rules: floral meristem development revealed by 3D gene expression atlases and high-resolution transcription factor–chromatin dynamics

“…promoter-reporter fusions with GUS or GFP) are largely identical to each other ( Peiffer et al., 2008 ). Because generating transgenic plants and crossing the transgene into different backgrounds (e.g., mutant backgrounds) is not required, in situ hybridization remains a powerful method for obtaining spatial information about RNA molecules ( Hu et al., 2023 ). A major limitation of in situ hybridization is its low throughput.…”

“…A recent study reported that LFY and AP1 mediate AP3 , PI , and AG activation by downregulating two zinc finger protein transcription factor genes, Arabidopsis ZINC FINGER PROTEIN1 ( ZP1 ), and ZINC FINGER PROTEIN8 ( ZFP8 ) ( Hu et al., 2023 ). ZP1 has known roles in proper root hair development, while ZP8 is associated with trichome initiation ( Hu et al., 2023 ). Hu and colleagues showed that ZP1 and ZFP8 are transcriptional repressors of AP3 , PI , and AG in leaves during the vegetative stage.…”

A new negative link in flower development: Repression of ABC genes by Z factors—ZP1/ZFP8

“…Only a very reduced subset of factors and interactions involved in flower development are shown––those most relevant to the work by Hu et al. ( 18 ). Novel interactions are depicted in blue.…”

“…In PNAS, Hu et al. ( 18 ) report the identification of specific C2H2 zinc finger TFs (ZINC FINGER PROTEIN1, ZP1, and ZINC FINGER PROTEIN 8, ZFP8) that are involved in the repression of AG , AP3, and PI in vegetative tissues and that are themselves down-regulated in developing flowers by LFY and AP1. That is, LFY and AP1, in addition to their role in directly activating in the floral primordia expression of the B and C class organ identity genes, would also up-regulate them indirectly: through the repression of their repressors, ZP1 and ZFP8 .…”