Mechanisms that chemically modify nucleosomes leading to inheritable activation or repression of pertinent genes are defined as epigenetic. H3K4me3 and H3K27me3 are interpreted as 'activating' and 'silencing' marks, respectively. Here, we demonstrate that even for related genes neither modification, alone, could serve as an indicator of expression status: despite being members of the same gene family selectively activated by ATX1, FLC and AP1 nucleosomes may be similarly decorated but, also, surprisingly different. 'Activating' H3K4me3 and 'silencing' H3K27me3 modifications co-exist at 5'-end nucleosomes of transcriptionally active FLC-gene, while highly transcribed AP1 displays neither of the two marks. The results suggest that distinct mechanisms 'read' and operate at each locus. In a remarkable contrast, H3K4me3-H3K27me3 profiles at downstream FLC and AP1 gene sequences remain unchanged and transmitted as stable marks throughout development. We propose that H3K4me3 and H3K27me3 produce a distinct bi-modular 'syllable' in the histone 'code' conveying different meaning on specific genes. Evidence that certain chromatin modifications might be common for active or non-active genome regions but, also, that the same histone signs might have gene-specific 'meaning', as reported here, might be critically important for large-scale genome analyses. ATX1 and CLF encode enzyme activities involved in establishing the H3K4me3 and H3K27me3 marks, respectively. The potential involvement of ATX1 and CLF in generating the dual H3K4me3 and H3K27me3 marks on FLC and AP1 nucleosomes was investigated.