Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway

Polycomb-group (PcG) proteins form a cellular memory by maintaining developmental regulators in a transcriptionally repressed state. We identified a novel flowering gene that is under PcG control in Arabidopsis--the MADS-box gene AGL19. AGL19 expression is maintained at very low levels by the PcG proteins MSI1, CLF, and EMF2, and AGL19 is partly responsible for the early flowering phenotype of clf mutants. AGL19 chromatin is strongly enriched in trimethylation of Lys 27 on histone H3 (H3K27me3) but not in H3K9me2. Repressive H3K27me3 marks were reduced by decreased CLF or MSI1 levels and by prolonged cold, suggesting that the PcG proteins MSI1 and CLF repress AGL19 in the absence of cold. Ectopic expression of AGL19 strongly accelerates flowering, and agl19 mutants have a decreased response to vernalization, the promotion of flowering by prolonged cold. Epistasis analyses revealed that AGL19 works in the poorly characterized FLC-independent vernalization pathway and does not require SOC1 to function. In this pathway, prolonged cold relieves AGL19 from PcG repression by a mechanism that requires VIN3 but not VRN2. Elevated AGL19 levels activate LFY and AP1 and eventually cause flowering.